The increase of pericyte population in human neuromuscular disorders supports their role in muscle regeneration in vivo

Journal of Pathology

Volumn 228, Issue 4, 2012, Pages 544-553

  Díaz Manera, Jordi ^a,b   Gallardo, Eduard ^a,b   De Luna, Noemi ^a,b   Navas, Miquel ^a,b   Soria, Laura ^a   Garibaldi, Matteo ^c   Rojas García, Ricard ^a,b   Tonlorenzi, Rossana ^d   Cossu, Giulio ^d,e   Illa, Isabel ^a,b,f  

^a UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^b CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED SOBRE ENFERMEDADES NEURODEGENERATIVAS CIBERNED   (Spain)

^c SAPIENZA UNIVERSITY OF ROME   (Italy)

^d SAN RAFFAELE HOSPITAL   (Italy)

^e MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^f HOSPITAL DE LA SANTA CREU I SANT PAU   (Spain)

Author keywords

Alkaline phosphatase; Mesoangioblasts; Muscle dystrophy; Muscle regeneration; Myopathies; Pericytes

Indexed keywords

ALKALINE PHOSPHATASE; MYOD PROTEIN; BIOLOGICAL MARKER; MYOD1 MYOGENIC DIFFERENTIATION PROTEIN; NERVE CELL ADHESION MOLECULE;

ADULT; ARTICLE; CELL DIFFERENTIATION; CELL POPULATION; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; MALE; MICROVASCULAR ENDOTHELIAL CELL; MONONUCLEAR CELL; MUSCLE BIOPSY; MUSCLE REGENERATION; MYOPATHY; MYOTUBE; NEUROMUSCULAR DISEASE; NEUROPATHY; PERICYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SATELLITE CELL; SKELETAL MUSCLE; UMBILICAL VEIN ENDOTHELIAL CELL; BIOPSY; CELL CULTURE; CYTOLOGY; METABOLISM; MIDDLE AGED; MUSCULAR DYSTROPHY; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; REGENERATION; SKELETAL MUSCLE SATELLITE CELL; CELL SELECTION; MUSCLE CELL;

ADULT; BIOLOGICAL MARKERS; BIOPSY; CELL DIFFERENTIATION; CELLS, CULTURED; FEMALE; HUMANS; MALE; MIDDLE AGED; MUSCLE FIBERS, SKELETAL; MUSCLE, SKELETAL; MUSCULAR DYSTROPHIES; MYOD PROTEIN; NEUROMUSCULAR DISEASES; PERICYTES; REGENERATION; SATELLITE CELLS, SKELETAL MUSCLE;

EID: 84871204057     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.4083     Document Type: Article

References (38)

1. Le Grand F, Rudnicki MA. Skeletal muscle satellite cells and adult myogenesis. Curr Opin Cell Biol 2007; 19: 628-633.
2. Wallace GQ, McNally EM. Mechanisms of muscle degeneration, regeneration, and repair in the muscular dystrophies. Annu Rev Physiol 2009; 71: 37-57.
3. Tedesco FS, Dellavalle A, Diaz-Manera J, et al. Repairing skeletal muscle: Regenerative potential of skeletal muscle stem cells. J Clin Invest 2010; 120: 11-19.
4. Ferrari G, Cusella-De Angelis G, Coletta M, et al. Muscle regeneration by bone marrow-derived myogenic progenitors. Science 1998; 279: 1528-1530.
5. Asakura A, Rudnicki MA. Side population cells from diverse adult tissues are capable of in vitro hematopoietic differentiation. Exp Hematol 2002; 30: 1339-1345.
6. Mitchell KJ, Pannerec A, Cadot B, et al. Identification and characterization of a non-satellite cell muscle resident progenitor during postnatal development. Nat Cell Biol 2010; 12: 257-266.
7. Torrente Y, Belicchi M, Sampaolesi M, et al. Human circulating AC133+ stem cells restore dystrophin expression and ameliorate function in dystrophic skeletal muscle. J Clin Invest 2004; 114: 182-195.
8. Diaz-Manera J, Touvier T, Dellavalle A, et al. Partial dysferlin reconstitution by adult murine mesoangioblasts is sufficient for full functional recovery in a murine model of dysferlinopathy. Cell Death Dis 2010; 1: E61.
9. Boldrin L, Muntoni F, Morgan JE. Are human and mouse satellite cells really the same? J Histochem Cytochem 58: 941-955.
10. Sampaolesi M, Blot S, D'Antona G, et al. Mesoangioblast stem cells ameliorate muscle function in dystrophic dogs. Nature 2006; 444: 574-579.
11. De Angelis L, Berghella L, Coletta M, et al. Skeletal myogenic progenitors originating from embryonic dorsal aorta coexpress endothelial and myogenic markers and contribute to postnatal muscle growth and regeneration. J Cell Biol 1999; 147: 869-878.
12. Sampaolesi M, Torrente Y, Innocenzi A, et al. Cell therapy of α- sarcoglycan null dystrophic mice through intra-arterial delivery of mesoangioblasts. Science 2003; 301: 487-492.
13. Palumbo R, Sampaolesi M, De Marchis F, et al. Extracellular HMGB1, a signal of tissue damage, induces mesoangioblast migration and proliferation. J Cell Biol 2004; 164: 441-449.
14. Dellavalle A, Sampaolesi M, Tonlorenzi R, et al. Pericytes of human skeletal muscle are myogenic precursors distinct from satellite cells. Nat Cell Biol 2007; 9: 255-267.
15. Dellavalle A, Maroli G, Covarello D, et al. Pericytes resident in postnatal skeletal muscle differentiate into muscle fibres and generate satellite cells. Nat Commun 2011; 2: 499.
16. Brooks BR. El Escorial World Federation of Neurology criteria for the diagnosis of amyotrophic lateral sclerosis. Subcommittee on Motor Neuron Diseases/Amyotrophic Lateral Sclerosis of the World Federation of Neurology Research Group on Neuromuscular Diseases and the El Escorial 'Clinical limits of amyotrophic lateral sclerosis' workshop contributors. J Neurol Sci 1994; 124: 96-107.
17. Maier F, Bornemann A. Comparison of the muscle fiber diameter and satellite cells frequency in human muscle biopsies. Muscle Nerve 1999; 22: 578-583.
18. Tonlorenzi R, Dellavalle A, Schnapp E, et al. Isolation and characterization of mesoangioblasts from mouse, dog, and human tissues. Curr Protoc Stem Cell Biol 2007; 2: Unit 2B 1.
19. de Luna N, Gallardo E, Soriano M, et al. Absence of dysferlin alters myogenin expression and delays human muscle differentiation in vitro. J Biol Chem 2006; 281: 17092-17098.
20. Safadi A, Livne E, Silbermann M, et al. Activity of alkaline phosphatase in rat skeletal muscle localized along the sarcolemma and endothelial cell membranes. J Histochem Cytochem 1991; 39: 199-203.
21. Hyldahl RD, Xin L, Hubal MJ, et al. Activation of nuclear factor- κB following muscle eccentric contractions in humans is localized primarily to skeletal muscle-residing pericytes. FASEB J 2011; 25: 2956-2966.
22. Cros D, Pearson C, Verity MA. Polymyositis-dermatomyositis: Diagnostic and prognostic significance of muscle alkaline phosphatase. Am J Pathol 1980; 101: 159-176.
23. Grim M, Carlson BM. Alkaline phosphatase and dipeptidylpeptidase IV staining of tissue components of skeletal muscle: A comparative study. J Histochem Cytochem 1990; 38: 1907-1912.
24. Engel WK, Cunningham GG. Alkaline phosphatase-positive abnormal muscle fibers of humans. J Histochem Cytochem 1970; 18: 55-57.
25. Armulik A, Genove G, Betsholtz C. Pericytes: Developmental, physiological, and pathological perspectives, problems, and promises. Dev Cell 2011; 21: 193-215.
26. Valero MC, Huntsman HD, Liu J, et al. Eccentric exercise facilitates mesenchymal stem cell appearance in skeletal muscle. PloS One 2012; 7: E29760.
27. Walsh FS, Dickson G. Generation of multiple N-CAM polypeptides from a single gene. BioEssays 1989; 11: 83-88.
28. Cashman NR, Covault J, Wollman RL, et al. Neural cell adhesion molecule in normal, denervated, and myopathic human muscle. Ann Neurol 1987; 21: 481-489.
29. Illa I, Leon-Monzon M, Dalakas MC. Regenerating and denervated human muscle fibers and satellite cells express neural cell adhesion molecule recognized by monoclonal antibodies to natural killer cells. Ann Neurol 1992; 31: 46-52.
30. Walsh FS, Moore SE. Expression of cell adhesion molecule, NCAM, in diseases of adult human skeletal muscle. Neurosci Lett 1985; 59: 73-78.
31. Schmidt A. The significance of the detection of alkaline phosphatase in the diagnosis of neuromuscular diseases. Biomed Biochim Acta 1986; 45: S115-117.
32. Benitez-Bribiesca L, De la Vega G. Occurrence of alkaline phosphatase-containing muscle fibers after denervation. J Histochem Cytochem 1971; 19: 691-692.
33. Connolly AM, Pestronk A, Planer GJ, et al. Congenital muscular dystrophy syndromes distinguished by alkaline and acid phosphatase, merosin, and dystrophin staining. Neurology 1996; 46: 810-814.
34. Christov C, Chretien F, Abou-Khalil R, et al. Muscle satellite cells and endothelial cells: Close neighbors and privileged partners. Mol Biol Cell 2007; 18: 1397-1409.
35. Murphy MM, Lawson JA, Mathew SJ, et al. Satellite cells, connective tissue fibroblasts and their interactions are crucial for muscle regeneration. Development 2011; 138: 3625-3637.
36. Lepper C, Partridge TA, Fan CM. An absolute requirement for Pax7-positive satellite cells in acute injury-induced skeletal muscle regeneration. Development 2011; 138: 3639-3646.
37. Sambasivan R, Yao R, Kissenpfennig A, et al. Pax7-expressing satellite cells are indispensable for adult skeletal muscle regeneration. Development 2011; 138: 3647-3656.
38. Abou-Khalil R, Le Grand F, Pallafacchina G, et al. Autocrine and paracrine angiopoietin 1/Tie-2 signaling promotes muscle satellite cell self-renewal. Cell Stem Cell 2009; 5: 298-309.