DOI: 10.4049/jimmunol.165.6.2997. Activin A Stimulates Type IV Collagenase (Matrix Metalloproteinase-2) Production in Mouse Peritoneal Macrophages

Activin A Stimulates Type IV Collagenase (Matrix Metalloproteinase-2) Production in Mouse Peritoneal Macrophages

10.4049/jimmunol.165.6.2997

Crossref journal-article

Oxford University Press (OUP)

The Journal of Immunology (286)

Abstract

Abstract The role of activin, a dimer of inhibin β subunit, in mouse peritoneal macrophages was evaluated. Activin activity in the cultured macrophages was augmented in response to activation by LPS. In Western blot analysis, immunoreactive activin A was detected in the culture medium only when the macrophages were stimulated by LPS. Although mRNA expression of βA subunit was detected, that of α and βB subunit was not found in macrophages by reverse RT-PCR. The activin βA mRNA level was increased in macrophages by LPS, suggesting that the activin production augmented by LPS is regulated at the mRNA level of the βA gene. The mRNAs of four activin receptors (ActRI, ActRIB, ActRII, and ActRIIB) were also detected in the peritoneal macrophages, and the mRNA levels, except for ActRIB, were decreased during the LPS treatment. Exogenous activin A stimulated the mRNA expression and gelatinolytic activity of matrix metalloproteinase-2 (MMP-2) in macrophages in both the presence and the absence of LPS. In contrast, activin did not affect the production of MMP-9 in macrophages. These results suggested that 1) mouse peritoneal macrophages produced activin A; 2) expression of activin A was enhanced with activation of the macrophages; 3) the macrophages also expressed activin receptors; and 4) exogenous activin A stimulated MMP-2 expression and activity, implicating activin A as an positive regulator of MMP-2 expression. Considering that MMP-2 constitutes the rate-limiting proteinase governing the degradation of basement membrane collagens, activin A may be involved in migration and infiltration of macrophages through the basement membrane in an inflammatory state.

Bibliography

Ogawa, K., Funaba, M., Mathews, L. S., & Mizutani, T. (2000). Activin A Stimulates Type IV Collagenase (Matrix Metalloproteinase-2) Production in Mouse Peritoneal Macrophages. The Journal of Immunology, 165(6), 2997â3003.

Authors 4

Kenji Ogawa (first)
Masayuki Funaba (additional)
Lawrence S. Mathews (additional)
Takeo Mizutani (additional)

References 52 Referenced 71

Dates

Type	When
Created	11 years, 4 months ago (April 20, 2014, 9:30 p.m.)
Deposited	8 months ago (Jan. 2, 2025, 2 p.m.)
Indexed	6 days, 20 hours ago (Aug. 29, 2025, 6:23 a.m.)
Issued	24 years, 11 months ago (Sept. 15, 2000)
Published	24 years, 11 months ago (Sept. 15, 2000)
Published Print	24 years, 11 months ago (Sept. 15, 2000)

Funders 0

None

BibTeX

@article{Ogawa_2000, title={Activin A Stimulates Type IV Collagenase (Matrix Metalloproteinase-2) Production in Mouse Peritoneal Macrophages}, volume={165}, ISSN={1550-6606}, url={http://dx.doi.org/10.4049/jimmunol.165.6.2997}, DOI={10.4049/jimmunol.165.6.2997}, number={6}, journal={The Journal of Immunology}, publisher={Oxford University Press (OUP)}, author={Ogawa, Kenji and Funaba, Masayuki and Mathews, Lawrence S. and Mizutani, Takeo}, year={2000}, month=sep, pages={2997–3003} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        8,
        29
      ]
    ],
    "date-time": "2025-08-29T10:23:31Z",
    "timestamp": 1756463011133,
    "version": "3.32.0"
  },
  "reference-count": 52,
  "publisher": "Oxford University Press (OUP)",
  "issue": "6",
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        2000,
        9,
        15
      ]
    ]
  },
  "abstract": "<jats:title>Abstract</jats:title>\n               <jats:p>The role of activin, a dimer of inhibin \u03b2 subunit, in mouse peritoneal macrophages was evaluated. Activin activity in the cultured macrophages was augmented in response to activation by LPS. In Western blot analysis, immunoreactive activin A was detected in the culture medium only when the macrophages were stimulated by LPS. Although mRNA expression of \u03b2A subunit was detected, that of \u03b1 and \u03b2B subunit was not found in macrophages by reverse RT-PCR. The activin \u03b2A mRNA level was increased in macrophages by LPS, suggesting that the activin production augmented by LPS is regulated at the mRNA level of the \u03b2A gene. The mRNAs of four activin receptors (ActRI, ActRIB, ActRII, and ActRIIB) were also detected in the peritoneal macrophages, and the mRNA levels, except for ActRIB, were decreased during the LPS treatment. Exogenous activin A stimulated the mRNA expression and gelatinolytic activity of matrix metalloproteinase-2 (MMP-2) in macrophages in both the presence and the absence of LPS. In contrast, activin did not affect the production of MMP-9 in macrophages. These results suggested that 1) mouse peritoneal macrophages produced activin A; 2) expression of activin A was enhanced with activation of the macrophages; 3) the macrophages also expressed activin receptors; and 4) exogenous activin A stimulated MMP-2 expression and activity, implicating activin A as an positive regulator of MMP-2 expression. Considering that MMP-2 constitutes the rate-limiting proteinase governing the degradation of basement membrane collagens, activin A may be involved in migration and infiltration of macrophages through the basement membrane in an inflammatory state.</jats:p>",
  "DOI": "10.4049/jimmunol.165.6.2997",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2014,
        4,
        21
      ]
    ],
    "date-time": "2014-04-21T01:30:49Z",
    "timestamp": 1398043849000
  },
  "page": "2997-3003",
  "source": "Crossref",
  "is-referenced-by-count": 71,
  "title": "Activin A Stimulates Type IV Collagenase (Matrix Metalloproteinase-2) Production in Mouse Peritoneal Macrophages",
  "prefix": "10.1093",
  "volume": "165",
  "author": [
    {
      "given": "Kenji",
      "family": "Ogawa",
      "sequence": "first",
      "affiliation": [
        {
          "name": "*Laboratory Animal Research Center, RIKEN, Wako, Saitama, Japan;"
        }
      ]
    },
    {
      "given": "Masayuki",
      "family": "Funaba",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "\u2020Department of Nutrition, Azabu University School of Veterinary Medicine, Sagamihara, Kanagawa, Japan; and"
        },
        {
          "name": "\u2021Department of Biological Chemistry, University of Michigan, Ann Arbor, MI 48109"
        }
      ]
    },
    {
      "given": "Lawrence S.",
      "family": "Mathews",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "\u2021Department of Biological Chemistry, University of Michigan, Ann Arbor, MI 48109"
        }
      ]
    },
    {
      "given": "Takeo",
      "family": "Mizutani",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "*Laboratory Animal Research Center, RIKEN, Wako, Saitama, Japan;"
        }
      ]
    }
  ],
  "member": "286",
  "reference": [
    {
      "key": "2023010117535962700_R1",
      "doi-asserted-by": "crossref",
      "unstructured": "Ying, S.-Y..  1988. Inhibins, activins and follistatins: gonadal proteins modulating the secretion of follicle stimulating hormone. Endocr. Rev.\u20089: 267",
      "DOI": "10.1210/edrv-9-2-267"
    },
    {
      "key": "2023010117535962700_R2",
      "doi-asserted-by": "crossref",
      "unstructured": "Vale, W.,  A. Hsueh,  C. Rivier,  J. Yu.  1990. The inhibin/activin family of hormones and growth factors.  M. A. Sporn,  ed. Peptide Growth Factors and Their Receptors. Handbook of Experimental Pharmacology\u2008211 Springer-Verlag,  Berlin.",
      "DOI": "10.1007/978-3-642-74781-6_8"
    },
    {
      "key": "2023010117535962700_R3",
      "doi-asserted-by": "crossref",
      "unstructured": "Murata, T.,  S.-Y. Ying.  1991. Transforming growth factor-\u03b2 and activin inhibit basal secretion of prolactin in pituitary monolayer culture system. Proc. Soc. Exp. Biol. Med.\u2008198: 599",
      "DOI": "10.3181/00379727-198-43295"
    },
    {
      "key": "2023010117535962700_R4",
      "doi-asserted-by": "crossref",
      "unstructured": "Bilezikjian, L. M.,  A. Z. Corrigan,  W. Vale.  1990. Activin A modulates growth hormone secretion from cultures of rat anterior pituitary cells. Endocrinology\u2008126: 2369",
      "DOI": "10.1210/endo-126-5-2369"
    },
    {
      "key": "2023010117535962700_R5",
      "doi-asserted-by": "crossref",
      "unstructured": "Schubert, D.,  H. Kimura,  M. LaCorbiere,  J. Vaughan,  D. Karr,  W. H. Fischer.  1990. Activin is a nerve cell survival molecule. Nature\u2008344: 868",
      "DOI": "10.1038/344868a0"
    },
    {
      "key": "2023010117535962700_R6",
      "doi-asserted-by": "crossref",
      "unstructured": "Hashimoto, M.,  S. Kondo,  T. Sakurai,  Y. Etoh,  H. Shibai,  M. Muramatsu.  1990. Activin/EDF as an inhibitor of neural differentiation. Biochem. Biophys. Res. Commun.\u2008173: 193",
      "DOI": "10.1016/S0006-291X(05)81040-X"
    },
    {
      "key": "2023010117535962700_R7",
      "doi-asserted-by": "crossref",
      "unstructured": "Hemmati-Brivanlou, A.,  D. A. Melton.  1994. Inhibition of activin receptor signaling promotes neuralization in Xenopus. Cell\u200877: 273",
      "DOI": "10.1016/0092-8674(94)90319-0"
    },
    {
      "key": "2023010117535962700_R8",
      "doi-asserted-by": "crossref",
      "unstructured": "Hemmati-Brivanlou, A.,  O. G. Kelly,  D. A. Melton.  1994. Follistatin, an antagonist of activin, is expressed in the Spemann organizer and displays direct neuralizing activity. Cell\u200877: 283",
      "DOI": "10.1016/0092-8674(94)90320-4"
    },
    {
      "key": "2023010117535962700_R9",
      "doi-asserted-by": "crossref",
      "unstructured": "Totsuka, Y.,  M. Tabuchi,  I. Kojima,  H. Shibai,  E. Ogata.  1988. A novel action of activin A: stimulation of insulin secretion in rat pancreatic islets. Biochem. Biophys. Res. Commun.\u2008156: 335",
      "DOI": "10.1016/S0006-291X(88)80845-3"
    },
    {
      "key": "2023010117535962700_R10",
      "doi-asserted-by": "crossref",
      "unstructured": "Mauduit, C.,  M. A. Chauvin,  E. dePeretti,  A. M. Morera,  M. Benahmed.  1991. Effect of activin A on dehydroepiandrosterone and testosterone secretion by primary immature porcine Leydig cells. Biol. Reprod.\u200845: 101",
      "DOI": "10.1095/biolreprod45.1.101"
    },
    {
      "key": "2023010117535962700_R11",
      "doi-asserted-by": "crossref",
      "unstructured": "Miro, F.,  C. D. Smyth,  S. G. Hillier.  1991. Development-related effects of recombinant activin on steroid synthesis in rat granulosa cells. Endocrinology\u2008129: 3388",
      "DOI": "10.1210/endo-129-6-3388"
    },
    {
      "key": "2023010117535962700_R12",
      "doi-asserted-by": "crossref",
      "unstructured": "Li, W.,  B. H. Yuen,  P. C. Leung.  1992. Inhibition of progestin accumulation by activin-A in human granulosa cells. J. Clin. Endocrinol. Metab.\u200875: 285",
      "DOI": "10.1210/jcem.75.1.1320053"
    },
    {
      "key": "2023010117535962700_R13",
      "doi-asserted-by": "crossref",
      "unstructured": "Letterio, J. J..  2000. Murine models define the role of TGF-\u03b2 as a master regulator of immune cell function. Cytokine Growth Factor Rev.\u200811: 81",
      "DOI": "10.1016/S1359-6101(99)00031-3"
    },
    {
      "key": "2023010117535962700_R14",
      "unstructured": "Wahl, S. M..  1999. TGF-\u03b2 in the evolution and resolution of inflammatory and immune processes. Microbes Infect.\u20081: 1247"
    },
    {
      "key": "2023010117535962700_R15",
      "doi-asserted-by": "crossref",
      "unstructured": "de Visser, K. E.,  W. M. Kast.  1999. Effects of TGF-\u03b2 on the immune system: implications for cancer immunotherapy. Leukemia\u200813: 1188",
      "DOI": "10.1038/sj.leu.2401477"
    },
    {
      "key": "2023010117535962700_R16",
      "doi-asserted-by": "crossref",
      "unstructured": "Letterio, J. J.,  A. B. Roberts.  1998. Regulation of immune responses by TGF-\u03b2. Annu. Rev. Immunol.\u200816: 137",
      "DOI": "10.1146/annurev.immunol.16.1.137"
    },
    {
      "key": "2023010117535962700_R17",
      "doi-asserted-by": "crossref",
      "unstructured": "Letterio, J. J., and A. B. Roberts. TGF-\u03b2: a critical modulator of immune cell function. Clin. Immunol. Immunopathol. 84:244.",
      "DOI": "10.1006/clin.1997.4409"
    },
    {
      "key": "2023010117535962700_R18",
      "unstructured": "Shao, L.,  N. L. Frigon, Jr,  D. W. Sehy,  A. L. Yu,  J. Lofgren,  R. Schwall,  J. Yu.  1992. Regulation of production of activin A in human marrow stromal cells and monocytes. Exp. Hematol.\u200820: 1235"
    },
    {
      "key": "2023010117535962700_R19",
      "doi-asserted-by": "crossref",
      "unstructured": "Eramaa, M.,  M. Hurme,  U. H. Stenman,  O. Ritvos.  1992. Activin A/erythroid differentiation factor is induced during human monocyte activation. J. Exp. Med.\u2008176: 1449",
      "DOI": "10.1084/jem.176.5.1449"
    },
    {
      "key": "2023010117535962700_R20",
      "doi-asserted-by": "crossref",
      "unstructured": "Yu, J.,  L. E. Shao,  N. L. Frigon, Jr,  J. Lofgren,  R. Schwall.  1996. Induced expression of the new cytokine, activin A, in human monocytes: inhibition by glucocorticoids and retinoic acid. Immunology\u200888: 368",
      "DOI": "10.1046/j.1365-2567.1996.d01-675.x"
    },
    {
      "key": "2023010117535962700_R21",
      "doi-asserted-by": "crossref",
      "unstructured": "Yamada, R.,  T. Suzuki,  M. Hashimoto,  Y. Eto,  K. Shiokawa,  M. Muramatsu.  1992. Induction of differentiation of the human promyelocytic cell line HL-60 by activin/EDF. Biochem. Biophys. Res. Commun.\u2008187: 79",
      "DOI": "10.1016/S0006-291X(05)81461-5"
    },
    {
      "key": "2023010117535962700_R22",
      "doi-asserted-by": "crossref",
      "unstructured": "Yamashita, N.,  T. Nakajima,  H. Takahashi,  H. Kaneoka,  Y. Mizushima,  T. Sakane.  1993. Effects of activin A on IgE synthesis and cytokine production by human peripheral mononuclear cells. Clin. Exp. Immunol.\u200894: 214",
      "DOI": "10.1111/j.1365-2249.1993.tb06003.x"
    },
    {
      "key": "2023010117535962700_R23",
      "doi-asserted-by": "crossref",
      "unstructured": "Toossi, Z.,  C. S. Hirsch,  B. D. Hamilton,  C. K. Knuth,  M. A. Friedlander,  E. A. Rich.  1997. Decreased production of TGF-\u03b21 by human alveolar macrophages compared with blood monocytes. J. Immunol.\u2008156: 3461",
      "DOI": "10.4049/jimmunol.156.9.3461"
    },
    {
      "key": "2023010117535962700_R24",
      "doi-asserted-by": "crossref",
      "unstructured": "Uchiyama, H.,  M. Asashima.  1992. Specific erythroid differentiation of mouse erythroleukemia cells by activins and its enhancement by retinoic acids. Biochem. Biophys. Res. Commun.\u2008187: 347",
      "DOI": "10.1016/S0006-291X(05)81499-8"
    },
    {
      "key": "2023010117535962700_R25",
      "doi-asserted-by": "crossref",
      "unstructured": "Albano, R. M.,  N. Groome,  J. C. Smith.  1993. Activins are expressed in preimplantation mouse embryos and in ES and EC cells and are regulated on their differentiation. Development\u2008117: 711",
      "DOI": "10.1242/dev.117.2.711"
    },
    {
      "key": "2023010117535962700_R26",
      "doi-asserted-by": "crossref",
      "unstructured": "Albano, R. M.,  R. Arkell,  R. S. Beddington,  J. C. Smith.  1994. Expression of inhibin subunits and follistatin during postimplantation mouse development: decidual expression of activin and expression of follistatin in primitive streak, somites and hindbrain. Development\u2008120: 803",
      "DOI": "10.1242/dev.120.4.803"
    },
    {
      "key": "2023010117535962700_R27",
      "doi-asserted-by": "crossref",
      "unstructured": "Ebner, R.,  H. Chen,  L. Shum,  S. Lawler,  A. L. Lee,  T. F. Zioncheck,  A. R. Lopez,  R. Derynck.  1993. Cloning of a type I TGF-\u03b2 receptor and its effect on TGF-\u03b2 binding to the type II receptor. Science\u2008260: 1334",
      "DOI": "10.1126/science.8388127"
    },
    {
      "key": "2023010117535962700_R28",
      "doi-asserted-by": "crossref",
      "unstructured": "Verschuern, K.,  N. Dewulf,  M. J. Goumans,  O. Lonnoy,  A. Freijen,  S. Grimsby,  K. Vande Spiegle,  P. ten Dijke,  A. Moren,  P. Vanscheeuwijck, et al\u20081995. Expression of type I and type IB receptors for activin in midgestation mouse embryos suggests distinct functions in organogenesis. Mech. Dev.\u200852: 109",
      "DOI": "10.1016/0925-4773(95)00395-H"
    },
    {
      "key": "2023010117535962700_R29",
      "doi-asserted-by": "crossref",
      "unstructured": "Mathews, L. S.,  W. W. Vale.  1991. Expression cloning of an activin receptor, a predicted serine kinase. Cell\u200865: 973",
      "DOI": "10.1016/0092-8674(91)90549-E"
    },
    {
      "key": "2023010117535962700_R30",
      "doi-asserted-by": "crossref",
      "unstructured": "Attisano, L.,  J. L. Wrana,  S. Cheifetz,  J. Massague.  1992. Novel activin receptors: distinct genes and alternative mRNA splicing generate a repertoire of serine/threonine kinase receptors. Cell\u200868: 97",
      "DOI": "10.1016/0092-8674(92)90209-U"
    },
    {
      "key": "2023010117535962700_R31",
      "doi-asserted-by": "crossref",
      "unstructured": "Reponen, P.,  C. Sahlberg,  P. Huhtala,  T. Hurskainen,  I. Thesleff,  K. Tryggvason.  1992. Molecular cloning of murine 72-kDa type IV collagenase and its expression during mouse development. J. Biol. Chem.\u2008267: 7856",
      "DOI": "10.1016/S0021-9258(18)42592-6"
    },
    {
      "key": "2023010117535962700_R32",
      "doi-asserted-by": "crossref",
      "unstructured": "Reponen, P.,  C. Sahlberg,  C. Munaut,  I. Thesleff,  K. Tryggvason.  1994. High expression of 92-kD type IV collagenase (gelatinase B) in the osteoclast lineage during mouse development. J. Cell Biol.\u2008124: 1091",
      "DOI": "10.1083/jcb.124.6.1091"
    },
    {
      "key": "2023010117535962700_R33",
      "doi-asserted-by": "crossref",
      "unstructured": "Sabath, D. E.,  H. E. Broome,  M. B. Prystowsky.  1990. Glyceraldehyde-3-phosphate dehydrogenase mRNA is a major interleukin 2-induced transcript in a cloned T-helper lymphocyte. Gene\u200891: 185",
      "DOI": "10.1016/0378-1119(90)90087-8"
    },
    {
      "key": "2023010117535962700_R34",
      "doi-asserted-by": "crossref",
      "unstructured": "Birkedal-Hansen, H.,  R. E. Taylor.  1982. Detergent-activation of latent collagenase and resolution of its component molecules. Biochem. Biophys. Res. Commun.\u2008107: 1173",
      "DOI": "10.1016/S0006-291X(82)80120-4"
    },
    {
      "key": "2023010117535962700_R35",
      "doi-asserted-by": "crossref",
      "unstructured": "Nakamura, T.,  K. Takio,  Y. Eto,  H. Shibai,  K. Titani,  H. Sugino.  1990. Activin-binding protein from rat ovary is follistatin. Science\u2008247: 836",
      "DOI": "10.1126/science.2106159"
    },
    {
      "key": "2023010117535962700_R36",
      "doi-asserted-by": "crossref",
      "unstructured": "Wang, Q. F.,  P. G. Farnworth,  H. G. Burger,  J. K. Findlay.  1990. Acute inhibitory effect of follicle stimulating hormone-suppressing protein (FSP) on gonadotropin-releasing secretion in cultured rat anterior pituitary cells. Mol. Cell. Endocrinol.\u200872: 33",
      "DOI": "10.1016/0303-7207(90)90237-3"
    },
    {
      "key": "2023010117535962700_R37",
      "doi-asserted-by": "crossref",
      "unstructured": "Kogawa, K.,  T. Nakamura,  K. Sugino,  K. Takio,  K. Titani,  H. Sugino.  1991. Activin-binding protein is present in pituitary. Endocrinology\u2008128: 1434",
      "DOI": "10.1210/endo-128-3-1434"
    },
    {
      "key": "2023010117535962700_R38",
      "doi-asserted-by": "crossref",
      "unstructured": "Meriggiola, M. C.,  K. D. Dahl,  J. P. Mather,  W. J. Bremner.  1994. Follistatin decreases activin-stimulated FSH secretion with no effect on GnRH-stimulated FSH secretion in prepubertal male monkeys. Endocrinology\u2008134: 1967",
      "DOI": "10.1210/endo.134.4.8137764"
    },
    {
      "key": "2023010117535962700_R39",
      "doi-asserted-by": "crossref",
      "unstructured": "Heldin, C. H.,  K. Miyazono,  P. ten Dijke.  1997. TGF-\u03b2 signalling from cell membrane to nucleus through SMAD proteins. Nature\u2008390: 465",
      "DOI": "10.1038/37284"
    },
    {
      "key": "2023010117535962700_R40",
      "doi-asserted-by": "crossref",
      "unstructured": "Matsuse, T.,  Y. Fukuchi,  Y. Eto,  H. Matsui,  T. Hosoi,  T. Oka,  E. Ohga,  T. Nagase,  H. Orimo.  1995. Expression of immunoreactive and bioactive activin A protein in adult murine lung after bleomycin treatment. Am. J. Respir. Cell. Mol. Biol.\u200813: 17",
      "DOI": "10.1165/ajrcmb.13.1.7541220"
    },
    {
      "key": "2023010117535962700_R41",
      "doi-asserted-by": "crossref",
      "unstructured": "Nishihara, T.,  Y. Ohsaki,  N. Ueda,  T. Koseki,  Y. Eto.  1995. Induction of apoptosis in B lineage cells by activin A derived from macrophages. J. Interferon Cytokine Res.\u200815: 509",
      "DOI": "10.1089/jir.1995.15.509"
    },
    {
      "key": "2023010117535962700_R42",
      "doi-asserted-by": "crossref",
      "unstructured": "DePaolo, L. V.,  M. Mercado,  Y. Guo,  N. Ling.  1993. Increased follistatin (activin-binding protein) gene expression in rat anterior pituitary tissue after ovariectomy may be mediated by pituitary activin. Endocrinology\u2008132: 2221",
      "DOI": "10.1210/endo.132.5.8477666"
    },
    {
      "key": "2023010117535962700_R43",
      "doi-asserted-by": "crossref",
      "unstructured": "Assoian, R. K.,  B. E. Fleurdelys,  H. C. Stevenson,  P. J. Miller,  D. K. Madtes,  E. W. Raines,  R. Ross,  M. B. Sporn.  1987. Expression and secretion of type \u03b2 transforming growth factor by activated human macrophages. Proc. Natl. Acad. Sci. USA\u200884: 6020",
      "DOI": "10.1073/pnas.84.17.6020"
    },
    {
      "key": "2023010117535962700_R44",
      "doi-asserted-by": "crossref",
      "unstructured": "Zhou, Y.,  R. Scamurra,  T. W. Molitor,  M. P. Murtaugh.  1992. Characterization of transforming growth factor-\u03b21 gene expression in porcine immune cells. Mol. Immunol.\u200829: 965",
      "DOI": "10.1016/0161-5890(92)90135-K"
    },
    {
      "key": "2023010117535962700_R45",
      "doi-asserted-by": "crossref",
      "unstructured": "Caniggia, I.,  S. J. Lye,  J. C. Cross.  1997. Activin is a local regulator of human cytotrophoblast cell differentiation. Endocrinology\u2008138: 3976",
      "DOI": "10.1210/endo.138.9.5403"
    },
    {
      "key": "2023010117535962700_R46",
      "doi-asserted-by": "crossref",
      "unstructured": "Xie, B.,  Z. Dong,  I. J. Fidler.  1994. Regulatory mechanisms for the expression of type IV collagenases/gelatinases in murine macrophages. J. Immunol.\u2008152: 3637",
      "DOI": "10.4049/jimmunol.152.7.3637"
    },
    {
      "key": "2023010117535962700_R47",
      "doi-asserted-by": "crossref",
      "unstructured": "Welgus, H. G.,  E. J. Campbell,  J. D. Cury,  A. Z. Eisen,  R. M. Senior,  S. M. Wilhelm,  G. I. Goldberg.  1990. Neutral metalloproteinases produced by human mononuclear phagocytes: enzyme profile, regulation, and expression during cellular development. J. Clin. Invest.\u200886: 1496",
      "DOI": "10.1172/JCI114867"
    },
    {
      "key": "2023010117535962700_R48",
      "doi-asserted-by": "crossref",
      "unstructured": "Tsunawaki, S.,  M. Sporn,  A. Ding,  C. Nathan.  1988. Deactivation of macrophages by transforming growth factor-\u03b2. Nature\u2008334: 260",
      "DOI": "10.1038/334260a0"
    },
    {
      "key": "2023010117535962700_R49",
      "doi-asserted-by": "crossref",
      "unstructured": "Bogdan, C.,  J. Paik,  Y. Vodovotz,  C. Nathan.  1992. Contrasting mechanisms for suppression of macrophages cytokine release by transforming growth factor-\u03b2 and interleukin-10. J. Biol. Chem.\u2008267: 23301",
      "DOI": "10.1016/S0021-9258(18)50091-0"
    },
    {
      "key": "2023010117535962700_R50",
      "doi-asserted-by": "crossref",
      "unstructured": "Shull, M. M.,  I. Ormsby,  A. B. Kier,  S. Pawlowski,  R. J. Diebold,  M. Yin,  R. Allen,  C. Sidman,  G. Proetzel,  D. Calvin, et al\u20081992. Targeted disruption of the mouse transforming growth factor-\u03b21 gene results in multifocal inflammatory disease. Nature\u2008359: 693",
      "DOI": "10.1038/359693a0"
    },
    {
      "key": "2023010117535962700_R51",
      "doi-asserted-by": "crossref",
      "unstructured": "Yaswen, L.,  A. B. Kulkarni,  T. Fredrickson,  B. Mittleman,  R. Schiffman,  S. Payne,  G. Longenecker,  E. Mozes,  S. Karlsson.  1996. Autoimmune manifestations in the transforming growth factor-\u03b21 knockout mouse. Blood\u200887: 1439",
      "DOI": "10.1182/blood.V87.4.1439.bloodjournal8741439"
    },
    {
      "key": "2023010117535962700_R52",
      "doi-asserted-by": "crossref",
      "unstructured": "Williams, A. O.,  A. D. Knapton,  A. Geiser,  J. J. Letterio,  A. B. Roberts.  1996. The liver in transforming growth factor-\u03b21 (TGF-\u03b21) null mutant mice. Ultrastruct. Pathol.\u200820: 477",
      "DOI": "10.3109/01913129609016352"
    }
  ],
  "container-title": "The Journal of Immunology",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://journals.aai.org/jimmunol/article-pdf/165/6/2997/1124918/2997.pdf",
      "content-type": "application/pdf",
      "content-version": "vor",
      "intended-application": "syndication"
    },
    {
      "URL": "https://journals.aai.org/jimmunol/article-pdf/165/6/2997/1124918/2997.pdf",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2025,
        1,
        2
      ]
    ],
    "date-time": "2025-01-02T19:00:47Z",
    "timestamp": 1735844447000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://journals.aai.org/jimmunol/article/165/6/2997/69779/Activin-A-Stimulates-Type-IV-Collagenase-Matrix"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        2000,
        9,
        15
      ]
    ]
  },
  "references-count": 52,
  "journal-issue": {
    "issue": "6",
    "published-print": {
      "date-parts": [
        [
          2000,
          9,
          15
        ]
      ]
    }
  },
  "URL": "http://dx.doi.org/10.4049/jimmunol.165.6.2997",
  "relation": {},
  "ISSN": [
    "0022-1767",
    "1550-6606"
  ],
  "subject": [],
  "published": {
    "date-parts": [
      [
        2000,
        9,
        15
      ]
    ]
  }
}