Abstract
Purpose
Pericytes were once thought only to aid in angiogenesis and blood pressure control. Gradually, the known functions of pericytes and other perivascular stem cells (PSC) have broadly increased. The following review article will summarize the known functions and importance of pericytes across disciplines of pathology, stem cell biology, and tissue engineering.
Methods
A literature review was performed for studies examining the importance of pericytes in pathology, stem cell biology, and tissue engineering.
Results
The importance of pericytes most prominently includes the identification of the perivascular identity of mesenchymal stem cells (or MSC). Now, pericytes and other PSC are known to display surface markers and multilineage differentiation potential of MSC. Accordingly, interest in the purification and use of PSC for mesenchymal tissue formation and regeneration has increased. Significant demonstration of in vivo efficacy in bone and muscle regeneration has been made in laboratory animals. Contemporaneously with the uncovering of an MSC identity for pericytes, investigators in tumour biology have found biologically relevant roles for pericytes in tumor formation, lymphovascular invasion, and perivascular tumor spread. As well, the contribution of pericytes to perivascular tumors has been examined (and debated), including glomus tumour, myopericytoma and solitary fibrous tumour/hemangiopericytoma. In addition, an expanding recognition of pericyte mimicry and perivascular tumour invasion has occurred, encompassing common malignancies of the brain and skin.
Conclusions
In summary, pericytes have a wide range of roles in health and disease. Pericytes are being increasingly studied for their role in tumour formation, growth and invasion. Likewise, the application of pericytes/PSC for mesenchymal tissue engineering is an expanding field of interest.
Similar content being viewed by others
References
Collett GDM, Canfield AE (2005) Angiogenesis and pericytes in the initiation of ectopic calcification. Circ Res 96:930–938
Doherty MJ, Canfield AE (1999) Gene expression during vascular pericyte differentiation. Crit Rev Eukaryot Gene Expr 9:1–17
Farrington-Rock C et al (2004) Chondrogenic and adipogenic potential of microvascular pericytes. Circulation 110:2226–2232
Crisan M et al (2008) A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell 3:301–313
Murray IR et al. (2013) Natural history of mesenchymal stem cells, from vessel walls to culture vessels. Cell Mol Life Sci CMLS. doi:10.1007/s00018-013-1462-6
Tang W et al (2008) White fat progenitor cells reside in the adipose vasculature. Science 322:583–586
Feng J, Mantesso A, De Bari C, Nishiyama A, Sharpe PT (2011) Dual origin of mesenchymal stem cells contributing to organ growth and repair. Proc Natl Acad Sci USA 108:6503–6508
Dellavalle A et al (2007) Pericytes of human skeletal muscle are myogenic precursors distinct from satellite cells. Nat Cell Biol 9:255–267
Corselli M et al (2012) The tunica adventitia of human arteries and veins as a source of mesenchymal stem cells. Stem Cells Dev 21:1299–1308
James AW et al (2012) Perivascular stem cells: a prospectively purified mesenchymal stem cell population for bone tissue engineering. Stem Cells Transl Med 1:510–519
James AW et al. (2012) Use of human perivascular stem cells for bone regeneration. J Vis Exp JoVE e2952. doi:10.3791/2952
Askarinam A et al (2013) Human perivascular stem cells show enhanced osteogenesis and vasculogenesis with Nel-like molecule I protein. Tissue Eng A 19:1386–1397
James AW et al (2012) An abundant perivascular source of stem cells for bone tissue engineering. Stem Cells Transl Med 1:673–684
Chen CW et al (2013) Human pericytes for ischemic heart repair. Stem Cells Dayt Ohio 31:305–316
Fletcher C, Unni K, Mertens F (2002) World Health Organization classification of tumours. IARC Press, Lyon
Weiss S, Goldblum J (2008) Enzinger and Weiss’s soft tissue tumors. Mosby Elsevier, Philadelphia
Weiss SW, Rao VK (1992) Well-differentiated liposarcoma (atypical lipoma) of deep soft tissue of the extremities, retroperitoneum, and miscellaneous sites. A follow-up study of 92 cases with analysis of the incidence of ‘dedifferentiation’. Am J Surg Pathol 16:1051–1058
Gombos Z, Zhang PJ (2009) Glomus tumor. Arch Pathol Lab Med 132:1448–1452
Shugart RR, Soule EH, Johnson EW Jr (1963) Glomus tumor. Surg Gynecol Obstet 117:334–340
Folpe AL, Fanburg-Smith JC, Miettinen M, Weiss SW (2001) Atypical and malignant glomus tumors: analysis of 52 cases, with a proposal for the reclassification of glomus tumors. Am J Surg Pathol 25:1–12
Porter PL, Bigler SA, McNutt M, Gown AM (1991) The immunophenotype of hemangiopericytomas and glomus tumors, with special reference to muscle protein expression: an immunohistochemical study and review of the literature. Mod Pathol Off J U S Can Acad Pathol Inc 4:46–52
Boyde A (1980) Diagnostic electron microscopy of tumours. F.N. Ghadially, Butterworth Co (Publishers) Ltd., London
Erlandson R (1994) Diagnostic transmission electron microscopy of tumors. Raven Press, New York
Boon LM, Mulliken JB, Enjolras O, Vikkula M (2004) Glomuvenous malformation (glomangioma) and venous malformation: distinct clinicopathologic and genetic entities. Arch Dermatol 140:971–976
Calduch L et al (2002) Familial generalized multiple glomangiomyoma: report of a new family, with immunohistochemical and ultrastructural studies and review of the literature. Pediatr Dermatol 19:402–408
Mentzel T, Dei Tos AP, Sapi Z, Kutzner H (2006) Myopericytoma of skin and soft tissues: clinicopathologic and immunohistochemical study of 54 cases. Am J Surg Pathol 30:104–113
Granter SR, Badizadegan K, Fletcher CD (1998) Myofibromatosis in adults, glomangiopericytoma, and myopericytoma: a spectrum of tumors showing perivascular myoid differentiation. Am J Surg Pathol 22:513–525
Enzinger FM, Smith BH (1976) Hemangiopericytoma. An analysis of 106 cases. Hum Pathol 7:61–82
Ceballos KM, Munk PL, Masri BA, O’Connell JX (1999) Lipomatous hemangiopericytoma: a morphologically distinct soft tissue tumor. Arch Pathol Lab Med 123:941–945
Nielsen GP, Dickersin GR, Provenzal JM, Rosenberg AE (1995) Lipomatous hemangiopericytoma. A histologic, ultrastructural and immunohistochemical study of a unique variant of hemangiopericytoma. Am J Surg Pathol 19:748–756
Crisan M, Corselli M, Chen WCW, Péault B (2012) Perivascular cells for regenerative medicine. J Cell Mol Med 16:2851–2860
Ide F, Obara K, Mishima K, Saito I, Kusama K (2005) Ultrastructural spectrum of solitary fibrous tumor: a unique perivascular tumor with alternative lines of differentiation. Virchows Arch Int J Pathol 446:646–652
Allt G, Lawrenson JG (2001) Pericytes: cell biology and pathology. Cells Tissues Organs 169:1–11
Baluk P, Hashizume H, McDonald DM (2005) Cellular abnormalities of blood vessels as targets in cancer. Curr Opin Genet Dev 15:102–111
Abramsson A et al (2002) Analysis of mural cell recruitment to tumor vessels. Circulation 105:112–117
Xian X et al (2006) Pericytes limit tumor cell metastasis. J Clin Invest 116:642–651
Jain RK (2005) Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy. Science 307:58–62
Lugassy C, Péault B, Wadehra M, Kleinman HK, Barnhill RL (2013) Could pericytic mimicry represent another type of melanoma cell plasticity with embryonic properties? Pigment Cell Melanoma Res 26:746–754
Lugassy C et al (2013) Pilot study on ‘pericytic mimicry’ and potential embryonic/stem cell properties of angiotropic melanoma cells interacting with the abluminal vascular surface. Cancer Microenviron Off J Int Cancer Microenviron Soc 6:19–29
Barnhill RL, Lugassy C (2004) Angiotropic malignant melanoma and extravascular migratory metastasis: description of 36 cases with emphasis on a new mechanism of tumour spread. Pathology (Phila) 36:485–490
Cheng L et al (2013) Glioblastoma stem cells generate vascular pericytes to support vessel function and tumor growth. Cell 153:139–152
Acknowledgements
Clinical specimens were recovered and presented with appropriate institutional approval, under University of California, Los Angeles IRB # 13–000918. The authors thank the staff of Translational Pathology Core Laboratory, and AS James for their excellent technical assistance. AWJ is supported by the UCLA Pathology Translational Research Fund. MM is supported by NIH MARC T34 GM008563.
Conflict of interest
The authors declare that they have no conflict of interest.
Author information
Authors and Affiliations
Corresponding authors
Rights and permissions
About this article
Cite this article
Mravic, M., Asatrian, G., Soo, C. et al. From pericytes to perivascular tumours: correlation between pathology, stem cell biology, and tissue engineering. International Orthopaedics (SICOT) 38, 1819–1824 (2014). https://doi.org/10.1007/s00264-014-2295-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00264-014-2295-0