Skip to main content
SpringerLink
Log in
Book cover

Cardiac Remodeling and Failure pp 485–499Cite as

Role of Mast Cells in Cardiovascular Disease

  • Chapter

Part of the book series: Progress in Experimental Cardiology ((PREC,volume 5))

Abstract

Increased numbers of mast cells have been reported in human hearts with end-stage cardiomyopathy and in animal models of myocardial infarction, hypertension, and chronic volume overload secondary to mitral regurgitation and aortocaval fistula. Because of these observations, mast cells have been implicated in the pathophysiology of these cardiovascular disorders. Mast cells are known to store and release a variety of biologically active mediators, including numerous cytokines (e.g.,TNF-α and IL-6) and proteases (e.g., tryptase, chymase, and stromelysin), many of which are potentially involved in activating matrix metalloproteinases (MMPs). Accordingly, in this review, the potential role of cardiac mast cells in MMP activation, thereby causing fibrillar collagen degradation and adverse cardiac remodeling is considered. In particular, the following topics are contemplated: 1) the origin of increased cardiac mast cell density; 2) the functional consequences of cardiac mast cell degranulation; 3) the relationship between mast cell density and MMP activity; 4) the contribution of mast cell derived TNF-α to myocardial remodeling; 5) the effect of pharmacological prevention of mast cell degranulation on myocardial remodeling; 6) the effect of mast cells on fibroblast function; 7) a possible role of atrial natriuretic peptide in initiating the mast cell-MMP activation cascade; and 8) future research questions.

This is a preview of subscription content, log in via an institution.

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   259.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   329.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   329.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Patella V, Marinò I, Arbustini E, Lamparter-Schummert B, Verga L, Adt M, Marone G. 1998. Stem cell factor in mast cells and increased mast cell density in idiopathic and ischemic cardiomyopathy. Circulation 97:971–978.

    Article  PubMed  CAS  Google Scholar 

  2. Patella V, De Crescenzo G, Lamparter-Schummert B, De Rosa G, Adt M, Marone G. 1997. Increased cardiac mast cell density and mediator release in patients with dilated cardiomyopathy. Inflamm Res 46:S31–S32.

    Article  PubMed  CAS  Google Scholar 

  3. Engels W, Reiters PHCM, Daemen MJAP, Smits JFM, Van der Vusse GJ. 1995. Transmural changes in mast cell density in rat heart after infarct induction in vivo. J Path 177:423–429.

    Article  PubMed  CAS  Google Scholar 

  4. Hara M, Ono K, Hwang MW, Iwasaki A, Okada M, Nakatani K, Sasayama S, Matsumori A. 2002. Evidence for a role of mast cells in the evolution to congestive heart failure. J Exp Med 195:375–381.

    Article  PubMed  CAS  Google Scholar 

  5. Olivetti G, Lagrasta C, Ricci R, Sonnenblick EH, Capasso JM, Anversa P. 1989. Long-term pressure-induced cardiac hypertrophy: capillary and mast cell proliferation. Am J Physiol Heart Circ Physiol 63:H1766–H1772.

    Google Scholar 

  6. Panizo A, Mindán FJP, Galindo MF, Cenarruzabeitia E, Hernández M, Díez J. 1995. Are mast cells involved in hypertensive heart disease? J Hypertens 13:1201–1208.

    Article  PubMed  CAS  Google Scholar 

  7. Dell’Italia LJ, Balcells E, Meng QC, Su X, Schultz D, Bishop SP, Machida N, Straeter-Knowlen IM, Hankes GH, Dillon R, Cartee ER, Oparil S. 1997. Volume-overload cardiac hypertrophy is unaffected by ACE inhibitor treatment in dogs. Am J Physiol Heart Circ Physiol 273:H961–H970.

    CAS  Google Scholar 

  8. Henegar JR, Thanigaraj S, Brower GL, Janicki JS. 1996. Myocardial mast cell response to chronic ventricular volume overload. J Mol Cell Cardiol 28:A202.

    Google Scholar 

  9. Bradding P, Okayama Y, Howarth PH, Church MK, Holgate ST. 1995. Heterogeneity of human mast cells based on cytokine content. J Immunol 155:297–307.

    PubMed  CAS  Google Scholar 

  10. Frangogiannis NG, Lindsey ML, Michael LH, Youker KA, Bressler RB, Mendoza LH, Spengler RN, Smith CW, Entman ML. 1998. Resident cardiac mast cells degranulate and release preformed TNF-alpha, initiating the cytokine cascade in experimental canine myocardial ischemia/reperfusion. Circulation 98:699–710.

    Article  PubMed  CAS  Google Scholar 

  11. Metcalfe DD, Baram D, Mekon YA. 1997. Mast cells. Physiol Rev 77:1033–1079.

    PubMed  CAS  Google Scholar 

  12. Nagase H. 1997. Activation mechanisms of matrix metalloproteinases. Biol Chem Hoppe Seyler 378:151–160.

    CAS  Google Scholar 

  13. Lees M, Taylor DJ, Woolley DE. 1994. Mast cell proteinases activate precursor forms of collagenase and stromelysin, but not of gelatinases A and B. Eur J Biochem 223:171–177.

    Article  PubMed  CAS  Google Scholar 

  14. Suzuki K, Lees M, Newlands GFJ, Nagase H, Woolley DE. 1995. Activation of precursors for matrix metalloproteinases 1 (interstitial collagenase) and 3 (stromelysin) by rat mast-cell proteinases I and II. Biochem J 305:301–306.

    PubMed  CAS  Google Scholar 

  15. Chakraborty A, Eghbali M. 1989. Collagenase activity in the normal rat myocardium. An immuno-histochemical method. Histochemistry 92:391–396.

    Article  PubMed  CAS  Google Scholar 

  16. Montfort I, Pérez-Tamayo R. 1975. The distribution of collagenase in normal rat tissues. J Histochem Cytochem 23:910–920.

    Article  PubMed  CAS  Google Scholar 

  17. Tyagi SC, Ratajska A, Weber KT 1993. Myocardial matrix metalloproteinase(s): localization and activation. Mol Cell Biochem 126:49–59.

    Google Scholar 

  18. Brower GL, Janicki JS. 2001. Contribution of ventricular remodeling to pathogenesis of heart failure in rats. Am J Physiol Heart Circ Physiol 280:H674–H683.

    PubMed  CAS  Google Scholar 

  19. Chancey AL, Brower GL, Peterson JT, Janicki JS. 2002. Effects of matrix metalloproteinase (MMP) inhibition on ventricular remodeling due to volume overload. Circulation 105; 1983–1988.

    Article  PubMed  CAS  Google Scholar 

  20. Coker ML, Thomas CV, Clair MJ, Hendrick JW, Krombach RS, Galis Z, Spinale FG. 1998. Myocardial matrix metalloproteinase activity and abundance with congestive heart failure. Am J Physiol Heart Circ Physiol 274:H1516–H1523.

    CAS  Google Scholar 

  21. Gunja-Smith Z, Morales AR, Romanelli R, Woessner JF, Jr. 1996. Remodeling of human myocardial collagen in idiopathic dilated cardiomyopathy—Role of metalloproteinases and pyridinoline cross-links. Am J Pathol 148:1639–1648.

    PubMed  CAS  Google Scholar 

  22. Janicki JS, Henegar JR, Campbell SE, Tyagi SC. 1995. Myocardial collagenase activity in experimental dilated cardiomyopathy. In: Wound Healing Responses in Cardiovascular Diseases. Ed. KT Weber. New York: Futura Press, pp. 73–81.

    Google Scholar 

  23. Spinale FG, Coker ML, Thomas CV, Walker JD, Mukherjee R, Hebbar L. 1998. Time-dependent changes in matrix metalloproteinase activity and expression during the progression of congestive heart failure—Relation to ventricular and myocyte function. Circ Res 82:482–495.

    Article  PubMed  CAS  Google Scholar 

  24. Tyagi SC, Campbell SE, Reddy HK, Tjahja E. Voelker DJ. 1996. Matrix metalloproteinase activity expression in infarcted, noninfarcted and dilated cardiomyopathic human hearts. Mol Cell Biochem 155:13–21.

    Article  PubMed  CAS  Google Scholar 

  25. Janicki JS, Matsubara BB. 1993. Myocardial collagen and left ventricular diastolic dysfunction. In: Left Ventricular Diastolic Dysfunction. Ed. WH Gaasch and MM LeWinter. Philadelphia: Lea Febiger. pp. 125–140.

    Google Scholar 

  26. Fernex M. 1968. The Mast Cell System: Its Relationship to Atherosclerosis, Fibrosis and Eosinophils. Baltimore: The Williams & Wilkins Company

    Google Scholar 

  27. Estensen RD. 1984. Eosinophilic myocarditis: a role for mast cells? Arch Pathol Lab Med 108:358–359.

    PubMed  CAS  Google Scholar 

  28. Dvorak AM. 1986. Mast-cell degranulation in human hearts. N Engl J Med 315:969–970.

    PubMed  CAS  Google Scholar 

  29. Li Q, Raza-Ahmad A, MacAulay MA, Lalonde LD, Rowden G, Trethewey E, Dean S. 1992. The relationship of mast cells and their secreted products to the volume of fibrosis in posttransplant hearts. Transplantation 53:1047–1051.

    Article  PubMed  CAS  Google Scholar 

  30. Kovanen PT. 1995. Role of mast cells in atherosclerosis. In: Human Basophils and Mast Cells: Clinical Aspects. Ed. G Marone. Chemical Immunology 62:132–170. Basel, Karger.

    Article  PubMed  CAS  Google Scholar 

  31. Brower GL, Henegar JR, Thanigaraj S, Janicki JS. 1996. Prevention of mast cell-induced myocardial collagenase activation in ventricular volume overload. Circulation 94:1–725.

    Article  Google Scholar 

  32. Frangogiannis NG, Perrard JL, Mendoza LH, Burns AR, Lindsey ML, Ballantyne CM, Michael LH, Smith CW, Entman ML. 1998. Stem cell factor induction is associated with mast cell accumulation after canine myocardial ischemia and reperfusion. Circulation 98:687–698.

    Article  PubMed  CAS  Google Scholar 

  33. Combs JW, Lagunoff D, Benditt EP. 1965. Differentiation and proliferation of embryonic mast cells of the rat. J Cell Biol 25:577–592.

    Article  PubMed  CAS  Google Scholar 

  34. Yong LC, Watkins S, Wilhelm DL. 1975. The mast cell: distribution and maturation in the peritoneal cavity of the adult rat. Pathology 7:307–318.

    Article  PubMed  CAS  Google Scholar 

  35. Yong LC, Watkins SG, Boland JE. 1979. The mast cell: III. Distribution and maturation in various organs of the young rat. Pathology 11:427–445.

    Article  PubMed  CAS  Google Scholar 

  36. Patella V, De Crescenzo G, Ciccarelli A, Marinò I, Adt M, Marone G. 1995. Human heart mast cells: A definitive case of mast cell heterogeneity. Int Arch Allergy Immunol 106:386–393.

    Article  PubMed  CAS  Google Scholar 

  37. Patella V, Marino I, Lampärter B, Arbustini E, Adt M, Marone G. 1995. Human heart mast cells: Isolation, purification, ultrastructure, and immunologic characterization. J Immunol 154:2855–2865.

    PubMed  CAS  Google Scholar 

  38. Brownell E, Fiorentino L, Jolly G, Wolfe K, Kincaid S, Seperack P, Visco D. 1995. Immunolocalization of stromelysin-related protein in murine mast cell granules. Int Arch Allergy Immunol 107:333–335.

    Article  PubMed  CAS  Google Scholar 

  39. Chancey AL, Brower GL, Janicki JS. 2002. Cardiac mast cell mediated activation of matrix metalloproteinases and alteration of ventricular diastolic function. Am J Physiol Heart Circ Physiol 282:H2152–H2158.

    PubMed  CAS  Google Scholar 

  40. Woessner JF, Jr. 1991. Matrix metalloproteinases and their inhibitors in connective tissue remodeling. FASEB J 5:2145–2154.

    PubMed  CAS  Google Scholar 

  41. Thomas CV, Coker ML, Zellner JL, Handy JR, Crumbley AJ, Spinale FG. 1998. Increased matrix metalloproteinase activity and selective upregulation in LV myocardium from patients with end-stage dilated cardiomyopathy. Circulation 97:1708–1715.

    Article  PubMed  CAS  Google Scholar 

  42. Dixon IM, Ju H, Reid NL, Scammell-La FT, Werner JP, Jasmin G. 1997. Cardiac collagen remodeling in the cardiomyopathic Syrian hamster and the effect of losartan. J Mol Cell Cardiol 29:1837–1850.

    Article  PubMed  CAS  Google Scholar 

  43. Janicki JS, Brower GL, Henegar JR. 1995. Interstitial collagen remodeling in chronic heart failure. Basic Applied Myology 5:339–348.

    Google Scholar 

  44. Senzaki H, Paolocci N, Gluzband YA, Lindsey ML, Janicki JS, Crow MT, Kass DA. 2000. β-blockade prevents sustained metalloproteinase activation and diastolic stiffening induced by angiotensin II combined with evolving cardiac dysfunction. Circ Res 86:807–815.

    Article  PubMed  CAS  Google Scholar 

  45. Spinale FG, Zellner JL, Johnson WS, Eble DM, Munyer PD. 1996. Cellular and extracellular remodeling with the development and recovery from tachycardia-induced cardiomyopathy: Changes in fibrillar collagen, myocyte adhesion capacity and proteoglycans. J Mol Cell Cardiol 28:1591–1608.

    Article  PubMed  CAS  Google Scholar 

  46. Brower GL, Chancey AL, Thanigaraj S, Matsubara BB, Janicki JS. 2002. A cause and effect relationship between myocardial mast cell number and matrix metalloproteinase activity. Am J Physiol Heart Circ Physiol 283:H518–H525.

    PubMed  CAS  Google Scholar 

  47. Stewart JA, Jr., Wei CC, Brower GL, Rynders PE, Hankes GH, Dillon AR, Lucchesi PA, Janicki JS, Dell’Italia LJ. 2003. Effects of experimental mitral regurgitation in dogs on cardiac mast cell density and MMP, chymase and ACE activity. Am J Physiol Heart Circ Physiol In Press.

    Google Scholar 

  48. Brower GL, Henegar JR, Janicki JS. 1996. Temporal evaluation of left ventricular remodeling and function in rats with chronic volume overload. Am J Physiol Heart Circ Physiol 271:H2071–H2078.

    CAS  Google Scholar 

  49. Bozkurt B, Kribbs SB, Clubb FJ, Jr., Michael LH, Didenko W, Hornsby PJ, Seta Y, Oral H, Spinale FG, Mann DL. 1998. Pathophysiologically relevant concentrations of tumor necrosis factor-a promote progressive left ventricular dysfunction and remodeling in rats. Circulation 97:1382–1391.

    Article  PubMed  CAS  Google Scholar 

  50. Armbrust T, Batusic D, Ringe B, Ramadori G. 1997. Mast cells distribution in human liver disease and experimental rat liver fibrosis. Indications for mast cell participation in development of liver fibrosis. Hepat 26:1042–1054.

    Article  CAS  Google Scholar 

  51. Berton A, Levi-Schaffer F, Emonard H, Garbuzenko E, Gillery P, Maquart FX. 2000. Activation of fibroblasts in collagen lattices by mast cell extract: a model of fibrosis. Clin Exp Allergy 30:485–492.

    Article  PubMed  CAS  Google Scholar 

  52. Cairns JA, Walls AF. 1997. Mast cell tryptase stimulates the synthesis of type I collagen in human lung fibroblasts. J Clin Invest 99:1313–1321.

    Article  PubMed  CAS  Google Scholar 

  53. Everett ET, Pablos JL, Harley RA, LeRoy EC, Norris JS. 1995. The role of mast cells in the development of skin fibrosis in tight-skin mutant mice. Comp Biochem Physiol [A] 110:159–165.

    Article  CAS  Google Scholar 

  54. de Almeida A, Mustin D, Forman MF, Brower GL, Janicki JS, Carver W 2002. Effects of mast cells on the behavior of isolated heart fibroblasts: modulation of collagen remodeling and gene expression. J Cell Physiol 191:51–59.

    Article  PubMed  Google Scholar 

  55. Brower GL, Janicki JS. 2003. Pharmacologic inhibition of mast cell degranulation prevents left ventricular remodeling induced by chronic volume overload in rats. Cardiovascular Research In Press.

    Google Scholar 

  56. Grundemar L, Krstenansky JL, Håkanson R. 1994. Neuropeptide Y and truncated neuropeptide Y analogs evoke histamine release from rat peritoneal mast cells. A direct effect on G proteins? Eur J Pharmacol 258:163–166.

    Article  PubMed  CAS  Google Scholar 

  57. Opgenorth TJ, Budzik GP, Mollison KW, Davidsen SK, Holst MR, Holleman WH. 1990. Atrial peptides induce mast cell histamine release. Peptides 11:1003–1007.

    Article  PubMed  CAS  Google Scholar 

  58. Yoshida H, Inagaki Y, Yamaki K, Beppu Y, Kawashima T, Takagi K. 1996. Histamine release induced by human natriuretic peptide from rat peritoneal mast cells. Regul Pept 61:45–49.

    Article  PubMed  CAS  Google Scholar 

  59. Huang M, Hester RL, Guyton AC. 1992. Hemodynamic changes in rats after opening an arteriovenous fistula. Am J Physiol Heart Circ Physiol 262:H846–H851.

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Anatomy, Physiology & Pharmacology, Auburn University, Auburn, Alabama, USA

    Joseph S. Janicki Ph.D, Gregory L. Brower, Amanda L. Chancey, Mary F. Forman & Lynetta J. Jobe

  2. Department of Developmental Biology and Anatomy, University of South Carolina, Columbia, South Carolina, USA

    Wayne Carver

Authors
  1. Joseph S. Janicki Ph.D
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gregory L. Brower
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Wayne Carver
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Amanda L. Chancey
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mary F. Forman
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Lynetta J. Jobe
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Joseph S. Janicki Ph.D .

Editor information

Editors and Affiliations

  1. Institute of Cardiovascular Sciences, St. Boniface General Hospital Research Centre, Faculty of Medicine, University of Manitoba, Winnipeg, Canada

    Pawan K. Singal PhD, DSc (Professor), Ian M. C. Dixon PhD (Associate Professor), Lorrie A. Kirshenbaum PhD (Associate Professor) & Naranjan S. Dhalla PhD, MD (HON), DSc (HON) (Distinguished Professor and Director) (Professor),  (Associate Professor),  (Associate Professor) &  (Distinguished Professor and Director)

Rights and permissions

Reprints and permissions

Copyright information

© 2003 Springer Science+Business Media New York

About this chapter

Cite this chapter

Janicki, J.S., Brower, G.L., Carver, W., Chancey, A.L., Forman, M.F., Jobe, L.J. (2003). Role of Mast Cells in Cardiovascular Disease. In: Singal, P.K., Dixon, I.M.C., Kirshenbaum, L.A., Dhalla, N.S. (eds) Cardiac Remodeling and Failure. Progress in Experimental Cardiology, vol 5. Springer, Boston, MA. https://doi.org/10.1007/978-1-4419-9262-8_33

Download citation

  • DOI: https://doi.org/10.1007/978-1-4419-9262-8_33

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4613-4864-1

  • Online ISBN: 978-1-4419-9262-8

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation