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(Circulation. 1996;94:1655-1664.)
© 1996 American Heart Association, Inc.

Articles

Adventitial Myofibroblasts Contribute to Neointimal Formation in Injured Porcine Coronary Arteries

Yi Shi, MD, PhD; James E. O'Brien, Jr, MD; Ali Fard, MD; John D. Mannion, MD; Dian Wang, BS; Andrew Zalewski, MD

the Departments of Medicine (Cardiology) and Surgery (Cardiothoracic Surgery) (J.E.O'B., J.D.M.), Thomas Jefferson University, Philadelphia, Pa.

Correspondence to Andrew Zalewski, MD, Cardiovascular Research Center, Division of Cardiology, Thomas Jefferson University, Suite 410N, 1025 Walnut St, Philadelphia, PA 19107.

Background The adventitia undergoes remodeling changes after a deep medial coronary injury. Because this process is associated with the formation of adventitial myofibroblasts, which resemble medial smooth muscle (SM) cells, we have examined myofibroblast involvement in the development of neointima.

Methods and Results In a porcine model, severe endoluminal coronary injury resulted in fibroblast proliferation and adventitial remodeling. Significant adventitial responses were associated with increased neointimal formation (P<.01). To examine the contribution of adventitial cells to the development of neointima, proliferating cells were labeled with bromodeoxyuridine (BrdU) at 12 and 24 hours after injury, and their subsequent localization was determined by immunohistochemistry (n=24). At 2 to 3 days after severe injury, the adventitia contained numerous BrdU-labeled cells (37±4%), whereas the media demonstrated infrequent labeled cells (4±1%). Adventitial cells lacked -SM actin and desmin, which distinguished them from medial SM cells. At 7 to 8 days, some labeled cells acquired characteristics of myofibroblasts expressing -SM actin. They were found to translocate to the gap between dissected media and contributed to the formation of neointima (76±19%). At 18 to 35 days, labeled cells were abundant in the neointima (86±5%). They showed uniform immunostaining for -SM actin but not for desmin, thereby differing from medial SM cells and blood-borne cells.

Conclusions This study demonstrates translocation of adventitial fibroblasts to neointima, their phenotypic modulation to myofibroblasts, and distinct characteristics of myofibroblasts within neointima after severe endoluminal coronary injury. These findings suggest the significance of vascular fibroblasts in the process of arterial repair.

Key Words: adventitia • myofibroblasts • remodeling • restenosis

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				E. Rodriguez, E. H. Lambert, M. G. Magno, and J. D. Mannion Contractile smooth muscle cell apoptosis early after saphenous vein grafting Ann. Thorac. Surg., October 1, 2000; 70(4): 1145 - 1152. [Abstract] [Full Text] [PDF]

				G. Li, Y.-F. Chen, S. S. Kelpke, S. Oparil, and J. A. Thompson Estrogen Attenuates Integrin-{beta}3-Dependent Adventitial Fibroblast Migration After Inhibition of Osteopontin Production in Vascular Smooth Muscle Cells Circulation, June 27, 2000; 101(25): 2949 - 2955. [Abstract] [Full Text] [PDF]

				H. Otani, H. Ohmiya, R. Hattori, H. Fujii, H. Ninomiya, M. Kido, H. Kawaguchi, M. Osako, H. Imamura, T. Ohta, et al. Potential role of vacuolar H+-adenosine triphosphatase in neointimal formation in cultured human saphenous vein J. Thorac. Cardiovasc. Surg., May 1, 2000; 119(5): 998 - 1007. [Abstract] [Full Text] [PDF]

				G. Li, S.-J. Chen, S. Oparil, Y.-F. Chen, and J. A. Thompson Direct In Vivo Evidence Demonstrating Neointimal Migration of Adventitial Fibroblasts After Balloon Injury of Rat Carotid Arteries Circulation, March 28, 2000; 101(12): 1362 - 1365. [Abstract] [Full Text] [PDF]

				I. Fishbein, J. Waltenberger, S. Banai, L. Rabinovich, M. Chorny, A. Levitzki, A. Gazit, R. Huber, U. Mayr, S. D. Gertz, et al. Local Delivery of Platelet-Derived Growth Factor Receptor-Specific Tyrphostin Inhibits Neointimal Formation in Rats Arterioscler Thromb Vasc Biol, March 1, 2000; 20(3): 667 - 676. [Abstract] [Full Text] [PDF]

				M. Overhaus, J. Heckenkamp, S. Kossodo, D. Leszczynski, and G. M. LaMuraglia Photodynamic Therapy Generates a Matrix Barrier to Invasive Vascular Cell Migration Circ. Res., February 18, 2000; 86(3): 334 - 340. [Abstract] [Full Text] [PDF]

				S. Patel, Y. Shi, R. Niculescu, E. H. Chung, J. L. Martin, and A. Zalewski Characteristics of Coronary Smooth Muscle Cells and Adventitial Fibroblasts Circulation, February 8, 2000; 101(5): 524 - 532. [Abstract] [Full Text] [PDF]

				A.-C. Desfaits, J. Raymond, and J. P. Muizelaar Growth Factors Stimulate Neointimal Cells In Vitro and Increase the Thickness of the Neointima Formed at the Neck of Porcine Aneurysms Treated by Embolization • Editorial Comment Stroke, February 1, 2000; 31(2): 498 - 507. [Abstract] [Full Text] [PDF]

				B. H. Strauss and M. Rabinovitch Adventitial Fibroblasts . Defining a Role in Vessel Wall Remodeling Am. J. Respir. Cell Mol. Biol., January 1, 2000; 22(1): 1 - 3. [Full Text]

				E. Faggin, M. Puato, A. Chiavegato, R. Franch, P. Pauletto, and S. Sartore Fish Oil Supplementation Prevents Neointima Formation in Nonhypercholesterolemic Balloon-Injured Rabbit Carotid Artery by Reducing Medial and Adventitial Cell Activation Arterioscler Thromb Vasc Biol, January 1, 2000; 20(1): 152 - 163. [Abstract] [Full Text] [PDF]

				S. Oparil, S.-J. Chen, Y.-F. Chen, J. N Durand, L. Allen, and J. A Thompson Estrogen attenuates the adventitial contribution to neointima formation in injured rat carotid arteries Cardiovasc Res, December 1, 1999; 44(3): 608 - 614. [Abstract] [Full Text] [PDF]

				G. Li, Y.-F. Chen, G. L. Greene, S. Oparil, and J. A. Thompson Estrogen Inhibits Vascular Smooth Muscle Cell-Dependent Adventitial Fibroblast Migration In Vitro Circulation, October 12, 1999; 100(15): 1639 - 1645. [Abstract] [Full Text] [PDF]

				D. D. Gutterman Adventitia-dependent influences on vascular function Am J Physiol Heart Circ Physiol, October 1, 1999; 277(4): H1265 - H1272. [Full Text] [PDF]

				M. R Dashwood, P. Noertersheuser, M. Kirchengast, and K. Munter Altered endothelin-1 binding following balloon angioplasty of pig coronary arteries: effect of the ETA receptor antagonist, LU 135252 Cardiovasc Res, August 1, 1999; 43(2): 445 - 456. [Abstract] [Full Text] [PDF]

				M Gyongyosi, P Yang, A Hassan, F Weidinger, H Domanovits, A Laggner, and D Glogar Arterial remodelling of native human coronary arteries in patients with unstable angina pectoris: a prospective intravascular ultrasound study Heart, July 1, 1999; 82(1): 68 - 74. [Abstract] [Full Text] [PDF]

				E. Faggin, M. Puato, L. Zardo, R. Franch, C. Millino, F. Sarinella, P. Pauletto, S. Sartore, and A. Chiavegato Smooth Muscle-Specific SM22 Protein Is Expressed in the Adventitial Cells of Balloon-Injured Rabbit Carotid Artery Arterioscler Thromb Vasc Biol, June 1, 1999; 19(6): 1393 - 1404. [Abstract] [Full Text] [PDF]

				Y. Shi, S. Patel, R. Niculescu, W. Chung, P. Desrochers, and A. Zalewski Role of Matrix Metalloproteinases and Their Tissue Inhibitors in the Regulation of Coronary Cell Migration Arterioscler Thromb Vasc Biol, May 1, 1999; 19(5): 1150 - 1155. [Abstract] [Full Text] [PDF]

				N. Shiota, H. Okunishi, S. Takai, I. Mikoshiba, H. Sakonjo, N. Shibata, and M. Miyazaki Tranilast Suppresses Vascular Chymase Expression and Neointima Formation in Balloon-Injured Dog Carotid Artery Circulation, March 2, 1999; 99(8): 1084 - 1090. [Abstract] [Full Text] [PDF]