Development of sensory innervation in rat tibia: Co-localization of CGRP and substance P with growth-associated protein 43 (GAP-43)

Journal of Anatomy

Volumn 207, Issue 2, 2005, Pages 135-144

  Gajda, Mariusz ^a   Litwin, Jan A ^a   Cichocki, Tadeusz ^a   Timmermans, Jean Pierre ^b   Adriaensen, Dirk ^b  

^a JAGIELLONIAN UNIVERSITY   (Poland)

^b UNIVERSITY OF ANTWERP   (Belgium)

Author keywords

Bone; Fetus; Immunohistochemistry; Ossification

Indexed keywords

CALCITONIN GENE RELATED PEPTIDE; NEUROMODULIN; NEUROPEPTIDE; SUBSTANCE P;

ANIMAL TISSUE; ARTICLE; BONE DEVELOPMENT; BONE MARROW; BONE MINERALIZATION; BONE REMODELING; CELL MATURATION; CONTROLLED STUDY; EPIPHYSIS; FEMALE; FETUS; GESTATION PERIOD; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MALE; NERVE GROWTH; NONHUMAN; OSSIFICATION; PERICHONDRIUM; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; SENSORY NERVE;

ANIMALS; ANIMALS, NEWBORN; BIOLOGICAL MARKERS; CALCITONIN GENE-RELATED PEPTIDE; EMBRYONIC DEVELOPMENT; FEMALE; GAP-43 PROTEIN; GESTATIONAL AGE; IMMUNOHISTOCHEMISTRY; MALE; MICROSCOPY, FLUORESCENCE; NEURONS, AFFERENT; OSTEOGENESIS; RATS; RATS, WISTAR; SUBSTANCE P; TIBIA; UBIQUITIN THIOLESTERASE;

EID: 23344437821     PISSN: 00218782     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1469-7580.2005.00434.x     Document Type: Article

References (41)

1. Adriaensen D, Scheuermann DW, Gajda M, Brouns I, Timmermans JP (2001) Functional implications of extensive new data on the innervation of pulmonary neuroepithelial bodies. Ital J Anat Embryol 106, 395-403.
2. Aro H, Eerola E, Aho AJ (1985) Fracture healing in paraplegic rats. Acta Orthop Scand 56, 228-232.
3. Bjurholm A, Kreicbergs A, Brodin E, Schultzberg M (1988) Substance P- and CGRP-immunoreactive nerves in bone. Peptides 9, 165-171.
4. Bjurholm A, Kreicbergs A, Schultzberg M (1989) Fixation and demineralization of bone tissue for immunohistochemical staining of neuropeptides. Calcif Tissue Int 45, 227-231.
5. Bjurholm A, Kreicbergs A, Dahlberg L, Schultzberg M (1990) The occurrence of neuropeptides at different stages of DBM-induced heterotopic bone formation. Bone Miner 10, 95-107.
6. Calvo W, Forteza-Vila J (1969) On the development of bone marrow innervation in new-born rats as studied with silver impregnation and electron microscopy. Am J Anat 126, 355-372.
7. Calvo W, Haas RJ (1969) Die Histogenese des Knochenmarks der Ratte: Nervale Versorgung, Knochenmarkstroma und ihre Beziehung zur Blutzellbildung [On the histogenesis of the bone marrow in the rat: innervation, stroma and their relations to hemopoiesis]. Z Zellforsch Mikrosk Anat 95, 377-395.
8. Edoff K, Hellman J, Persliden J, Hildebrand C (1997) The developmental skeletal growth in the rat foot is reduced after denervation. Anat Embryol 195, 531-538.
9. Edoff K, Granseth B (2001) Neuropeptide content and physiological properties of rat cartilage-projecting sensory neurones co-cultured with perichondrial cells. Neurosci Lett 315, 141-144.
10. Edoff K, Hildebrand C (2003) Neuropeptide effects on rat chondrocytes and perichondrial cells in vitro. Neuropeptides 37, 316-318.
11. Ferguson C, Alpern E, Miclau T, Helms JA (1999) Does adult fracture repair recapitulate embryonic skeletal formation? Mech Dev 87, 57-66.
12. Fristad I, Vandevska-Radunovic V, Fjeld K, Wimalawansa SJ, Hals K, I (2003) NK1, NK2, NK3 and CGRP1 receptors identified in rat oral soft tissues, and in bone and dental hard tissue cells. Cell Tissue Res 311, 383-391.
13. Gajda M, Adriaensen D, Cichocki T (2000) Development of the innervation of long bones: expression of the growth-associated protein 43. Folia Histochem Cytobiol 38, 103-110.
14. Gajda M, Litwin JA, Adriaensen D, Timmermans JP, Cichocki T (2004) Segmental distribution and morphometric features of primary sensory neurons projecting to the tibial periosteum in the rat. Folia Histochem Cytobiol 42, 95-99.
15. Gilles FH, French JH (1961) Postinjection sciatic nerve palsies in infants and children. J Pediatr 58, 195-204.
16. Gillespie JA (1954) The nature of the bone changes associated with nerve injuries and disuse. J Bone Joint Surg Br 36, 464-473.
17. Hara-Irie F, Amizuka N, Ozawa H (1996) Immunohistochemical and ultrastructural localization of CGRP-positive nerve fibers at the epiphyseal trabecules facing the growth plate of rat femurs. Bone 18, 29-39.
18. Hill EL, Elde R (1991) Distribution of CGRP-, VIP-, DβH-, SP-, and NPY-immunoreactive nerves in the periosteum of the rat. Cell Tissue Res 264, 469-480.
19. Holzer P (1988) Local effector functions of capsaicin-sensitive sensory nerve endings: involvement of tachykinins, calcitonin gene-related peptide and other neuropeptides. Neuroscience 24, 739-768.
20. Hukkanen M, Konttinen YT, Santavirta S, et al. (1993) Rapid proliferation of calcitonin gene-related peptide-immunoreactive nerves during healing of rat tibial fracture suggests neural involvement in bone growth and remodelling. Neuroscience 54, 969-979.
21. Hukkanen M, Konttinen YT, Santavirta S, et al. (1995) Effect of sciatic nerve section on neural ingrowth into the rat tibial fracture callus. Clin Orthop 311, 247-257.
22. Imai S, Rauvala H, Konttinen YT, et al. (1997) Efferent targets of osseous CGRP-immunoreactive nerve fiber before and after bone destruction in adjuvant arthritic rat: an ultramorphological study on their terminal-target relations. J Bone Miner Res 12, 1018-1027.
23. Jackman A, Fitzgerald M (2000) Development of peripheral hindlimb and central spinal cord innervation by subpopulations of dorsal root ganglion cells in the embryonic rat. J Comp Neurol 418, 281-298.
24. Kuntz A, Richins CA (1945) Innervation of the bone marrow. J Comp Neurol 83, 213-221.
25. Li J, Ahmad T, Spetea M, Ahmed M, Kreicbergs A (2001) Bone reinnervation after fracture: a study in the rat. J Bone Miner Res 16, 1505-1510.
26. Mach DB, Rogers SD, Sabino MC, et al. (2002) Origins of skeletal pain: sensory and sympathetic innervation of the mouse femur. Neuroscience 113, 155-166.
27. Madsen JE, Hukkanen M, Aune AK, et al. (1998) Fracture healing and callus innervation after peripheral nerve resection in rats. Clin Orthop 351, 230-240.
28. Mbiene JP, Mistretta CM (1997) Initial innervation of embryonic rat tongue and developing taste papillae: nerves follow distinctive and spatially restricted pathways. Acta Anat 160, 139-158.
29. Miller MR, Kasahara M (1963) Observations on the innervation of human long bones. Anat Rec 145, 13-23.
30. Nordsletten L, Madsen JE, Almaas R, et al. (1994) The neuronal regulation of fracture healing. Effects of sciatic nerve resection in rat tibia. Acta Orthop Scand 65, 299-304.
31. Oestreicher AB, De Graan PN, Gispen WH, Verhaagen J, Schrama LH (1997) B-50, the growth associated protein-43: modulation of cell morphology and communication in the nervous system. Prog Neurobiol 53, 627-686.
32. Ring PA (1961) The influence of the nervous system upon the growth of bones. J Bone Joint Surg Br 43, 121-140.
33. Shih C, Bernard GW (1997a) Calcitonin gene related peptide enhances bone colony development in vitro. Clin Orthop 334, 335-344.
34. Shih C, Bernard GW (1997b) Neurogenic substance P stimulates osteogenesis in vitro. Peptides 18, 323-326.
35. Sisask G, Bjurholm A, Ahmed M, Kreicbergs A (1995) Ontogeny of sensory nerves in the developing skeleton. Anat Rec 243, 234-240.
36. Sisask G, Bjurholm A, Ahmed M, Kreicbergs A (1996) The development of autonomic innervation in bone and joints of the rat. J Auton Nerv Syst 59, 27-33.
37. Thurston TJ (1982) Distribution of nerves in long bones as shown by silver impregnation. J Anat 134, 719-728.
38. Vignery A, McCarthy TL (1996) The neuropeptide calcitonin gene-related peptide stimulates insulin-like growth factor I production by primary fetal rat osteoblasts. Bone 18, 331-335.
39. Villa I, Dal Fiume C, Maestroni A, Rubinacci A, Ravasi F, Guidobono F (2003) Human osteoblast-like cell proliferation induced by calcitonin-related peptides involves PKC activity. Am J Physiol Endocrinol Metab 284, E627-E633.
40. Wu Z, Nagata K, Iijima T (2002) Involvement of sensory nerves and immune cells in osteophyte formation in the ankle joint of adjuvant arthritic rats. Histochem Cell Biol 118, 213-220.
41. Zaidi M, Fuller K, Bevis PJ, Gaines Das RE, Chambers TJ, MacIntyre I (1987) Calcitonin gene-related peptide inhibits osteoclastic bone resorption: a comparative study. Calcif Tissue Int 40, 149-154.