Differential detection of impact site versus rotational site injury by magnetic resonance imaging and microglial morphology in an unrestrained mild closed head injury model

Journal of Neurochemistry

Volumn 136, Issue , 2016, Pages 18-28

  Hernandez, Alfredo ^a,b   Donovan, Virgina ^a,b,c   Grinberg, Yelena Y ^a   Obenaus, Andre ^a,c,d   Carson, Monica J ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c LOMA LINDA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d LOMA LINDA UNIVERSITY   (United States)

Author keywords

confocal microscopy; neuroinflammation; T2 weighted imaging; traumatic brain injury

Indexed keywords

CD40 ANTIGEN; CD45 ANTIGEN; HLA ANTIGEN CLASS 2; MOLECULAR MARKER; PURINERGIC P2Y12 RECEPTOR; TRIGGERING RECEPTOR EXPRESSED ON MYELOID CELLS 1; TRIGGERING RECEPTOR EXPRESSED ON MYELOID CELLS 2;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN EDEMA; BRAIN REGION; CELL ACTIVATION; CELL STRUCTURE; CONTROLLED STUDY; DISEASE SEVERITY; HEAD INJURY; IMAGE ANALYSIS; IMMUNOCOMPETENT CELL; MALE; MICROGLIA; MILD CLOSED HEAD INJURY; MOUSE; NEUROIMAGING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; PROTEIN EXPRESSION; TISSUE INJURY; ANIMAL; C57BL MOUSE; CONFOCAL MICROSCOPY; DISEASE MODEL; METABOLISM; PATHOLOGY; PROCEDURES; TRANSGENIC MOUSE;

ANIMALS; DISEASE MODELS, ANIMAL; HEAD INJURIES, CLOSED; MAGNETIC RESONANCE IMAGING; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROGLIA; MICROSCOPY, CONFOCAL;

EID: 84956773530     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.13402     Document Type: Article

References (43)

1. Amadio S., Parisi C., Montilli C., Carrubba A. S., Apolloni S., and, Volonté C., (2014) P2Y12 receptor on the verge of a neuroinflammatory breakdown. Mediators Inflamm. 2014, 975849. doi: 10.1155/2014/975849.
2. Bianchi A., Bhanu B., and, Obenaus A., (2015) Dynamic low-level context for the detection of mild traumatic brain injury. IEEE Trans. Biomed. Eng. 62, 145-153.
3. Butovsky O., Jedrychowski M. P., Moore C. S., et al,. (2014) Identification of a unique TGF-β-dependent molecular and functional signature in microglia. Nat. Neurosci. 17, 131-143.
4. Bye N., Habgood M. D., Callaway J. K., Malakooti N., Potter A., Kossmann T., and, Morganti-Kossmann M. C., (2007) Transient neuroprotection by minocycline following traumatic brain injury is associated with attenuated microglial activation but no changes in cell apoptosis or neutrophil infiltration. Exp. Neurol. 4, 220-233.
5. Carson M. J., Doose J. M., Melchior B., Schmid C. D., and, Ploix C. C., (2007) CNS immune privilege: hiding in plain sight. Immunol. Rev. 213, 48-65.
6. Carson M. J., Reilly C. R., Sutcliffe J. G., and, Lo D., (1998) Mature microglia resemble immature antigen presenting cells. Glia 22, 72-85.
7. Carson M. J., Thrash J. C., and, Walter B., (2006) The cellular response in neuroinflammation: The role of leukocytes, microglia and astrocytes in neuronal death and survival. Clin. Neurosci. Res. 6, 237-245.
8. Choy M., Dubé C. M., Patterson K., Barnes S. R., Maras P., Blood A. B., Hasso A. N., Obenaus A., and, Baram T. Z., (2014) A novel, noninvasive, predictive epilepsy biomarker with clinical potential. J. Neurosci. 34, 8672-8684.
9. Conde J. R., and, Streit W. J., (2006) Microglia and the aging brain. J. Neuropathol. Exp. Neurol. 65, 199-203.
10. Davalos D., Grutzendler J., Yang G., Kim J. V., Zuo Y., Jung S., Littman D. R., Dustin M. L., and, Gan W. B., (2005) ATP mediates rapid microglial response to local brain injury in vivo. Nat. Neurosci. 8, 752-758.
11. Donovan V., Bianchi A., Hartman R., Bhanu B., Carson M.J., Obenaus A., and (2014) Computational analysis reveals increased blood deposition following repeated mild traumatic grain injury. NeuroImage: Clinical. 1, 18-28.
12. Faul M., and, Coronado V., (2015) Epidemiology of traumatic brain injury and book of clinical neurology. Handb Clin Neurol. 127, 3-13.
13. Faul M., Xu L., Wald M. M., and, Coronado V., (2015) Traumatic Brain Injury in the United States: Emergency Visits Hospitalizations, and Deaths 2002-2006. Atlanta, GA. CDC, National Center for Injury Prevention and Control.
14. Fenn A. M., Gensel J. C., Huang Y., Popovich P. G., Lifshitz J., and, Godbout J. P., (2014) Immune activation promotes depression 1 month after diffuse brain injury: a role for primed microglia. Biol. Psychiatry 76, 575-584.
15. Gardner R. C., (2015) Yaffe K Epidemiology of mild traumatic brain injury and neurodegenerative disease. Mol. Cell Neurosci. 66, 75-80.
16. Gerriets T., Stolz E., Walberer M., Müller C., Rottger C., Kluge A., Kaps M., Fisher M., and, Bachmann G., (2004) Complications and pitfalls in rat stroke models for middle cerebral artery occlusion: a comparison between the suture and the macrosphere model using magnetic resonance angiography. Stroke 35, 2372-2377.
17. Hama H, Kurokawa H, Kawano H, Ando R, Shimogori T, Noda H, Fukami K, Sakaue-Sawano A, and, Miyawaki A., (2011) Scale: a chemical approach for fluorescence imaging and reconstruction of transparent mouse brain. Nature Neurosci. 14, 1481-1488.
18. Hickman S. E., Kingery N. D., Ohsumi T. K., Borowsky M. L., Wang L. C., Means T. K., and, El Khoury J., (2013) The microglial sensome revealed by direct RNA sequencing. Nat. Neurosci. 16, 1896-1905.
19. Huang L., Coats J. S., Mohd-Yusof A, et al,. (2013) Tissue Vulnerability is increased following repetitive mild traumatic brain injury in the rat. Brain Res. 1499: 109-120.
20. Irimia A., Chambers M. C., Alger J. R., et al,. (2011) Comparison of acute and chronic traumatic brain injury using semi-automatic multimodal segmentation of MR volumes. J. Neurotrauma 28, 2287-2306.
21. Jung S., Aliberti J., Graemmel P., Sunshine M. J., Kreutzberg G. W., Sher A., and, Littman D. R., (2000) Analysis of fractalkine receptor CX(3)CR1 function by targeted deletion and green fluorescent protein reporter gene insertion. Mol. Cell. Biol. 20, 4106-4114.
22. Kochanek P. M., Marion D. W., Zhang W., et al,. (1995) Severe controlled cortical impact in rats: assessment of cerebral edema, blood flow, and contusion volume. J. Neurotrauma 12, 1015-1025.
23. Loane D. J., Stoica B. A., Tchantchou F., Kumar A., Barrett J. P., Akintola T., Xue F., Conn P. J., and, Faden A. I., (2014) Novel mGluR5 positive allosteric modulator improves functional recovery, attenuates neurodegeneration, and alters microglial polarization after experimental traumatic brain injury. Neurotherapeutics 11, 857-869.
24. Melchior B., Garcia A. E., Hsiung B., Lo K. M., Doose J. M., Thrash J. C., Stalder A. K., Staufenbiel M., Neumann H., and, Carson M. J., (2010) Dual induction of TREM2 and tolerance-related transcript, Tmem176b, in amyloid transgenic mice: implications for vaccine-based therapies for Alzheimer's disease. ASN Neuro. 2, 157-170.
25. Mierzwa A. J., Sullivan G. M., Beer L. A., Ahn S., and, Armstrong R. C., (2014) Comparison of cortical and white matter traumatic brain injury models reveals differential effects in the subventricular zone and divergent Sonic hedgehog signaling pathways in neuroblasts and oligodendrocyte progenitors. ASN Neuro. 6: pii: 1759091414551782
26. Morganti-Kossman M. C., Rancan M., Otto V. I., Stahel P. F., and, Kossmann T., (2001) Role of cerebral Inflammation after brain injury: a revisited concept. Shock 16, 165-177
27. Mouzon B. C., Bachmeier C., Ferro A., Ojo J. O., Crynen G., Acker C. M., Davies P., Mullan M., Stewart W., and, Crawford F., (2014) Chronic neuropathological and neurobehavioral changes in a repetitive mild traumatic brain injury model. Ann. Neurol. 75, 241-254.
28. Nimmerjahn A., and, Kirchhoff F., (2005) Helmchen F Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 308, 1314-1318.
29. Obenaus A., (2015) Traumatic brain injury, in Encyclopedia of Mental Health, 2nd edition, Vol 4 (, Friedman H. S., Editor in Chief), pp. 329-340. Academic Press, Waltham, MA.
30. Obenaus A., Robbins M., Blanco G., Galloway N. R., Snissarenko E., Gillard E., Lee S., and, Currás-Collazo M., (2007) Multimodal magnetic resonance imaging alternations in two rat models of mild neurotrauma. J. Neurotrauma 24, 1147-1160.
31. Ojo J., Mouzon B. C., and, Crawford F., (2015) Repetitive head trauma, chronic traumatic encephalopathy and tau: challenges in translating from mice to men. Exp. Neurol. pii: S0014-4886(15)30015-7. doi: 10.1016/j.expneurol.2015.06.003. [Epub ahead of print]
32. Pacifico A., Amyot F., Arciniegas D., et al,. (2015) A review of the effectiveness of neuroimaging modalities for the detection of traumatic brain injury. J. Neurotrauma 32(22):1693-1721. doi: 10.1089/neu.2013.3306. Epub 2015 Sep 30.
33. Puntambekar S. S., Davis D. S., Hawel L., Crane J., Byus C. V., and, Carson M. J., (2011) LPS-induced CCR2 expression and macrophage influx into the murine central nervous system is polyamine-dependent. Brain Behav. Immun. BBI 25, 883-896.
34. Rancan M., Bye N., Otto V. I., Trentz O., Kossmann T., Frentzel S., and, Morganti-Kossmann M. C., (2004) The chemokine fractalkine in patients with severe traumatic brain injury and a mouse model of closed head injury. J. Cereb. Blood Flow Metab. 24, 1110-1118.
35. Roth T. L., Nayak D., Atanasijevic T., Koretsky A. P., Latour L. L., and, McGavern D. B., (2014) Transcranial amelioration of inflammation and cell death after brain injury. Nat. Neurosci. 505, 223-228.
36. Rutgers D. R., Toulgoat F., Cazejust J., Fillard P., Lasjaunias P., and, Ducreux D., (2008) White matter abnormalities in mild traumatic brain injury: a diffusion tensor imaging study. Am. J. Neuroradiol. 29 (3), 514-519.
37. Sakhon O. S., Ross B., Gusti V., Pham A. J., Vu K., and, Lo D. D., (2015) M cell-derived vesicles suggest a unique pathway for trans-epithelial antigen delivery. Tissue Barriers 3 (1-2), e1004975. doi: 10.1080/21688370.2015.1004975.
38. Schmid C. D., Melchior B., Masek K., Puntambeker S. S., Danielson P. E., Lo D. D., Sutcliffe J. G., and, Carson M. J., (2009) Differential gene expression in LPS/IFNgamma activated microglia and macrophages: in vitro versus in vivo. J. Neurochem. 109 s1, 117-125.
39. Schmid C. D., Sautkulis L. N., Danielson P. E., Cooper J., Hasel K. W., Hilbush B. S., Sutcliffe J. G., and, Carson M. J., (2002) Heterogeneous expression of the Triggering Receptor Expressed on Myeloid cells-2 (TREM-2) on adult murine microglia. J. Neurochem. 83, 1309-1320.
40. Smith C., Gentleman S. M., Leclercq P. D., Murray L. S., Griffin W. S., Graham D. I., and, Nicoll J. A., (2013) The neuroinflammatory response in humans after traumatic brain injury. Neuropathol. Appl. Neurobiol. 39, 654-666.
41. Susarla B. T., Villapol S., Yi J. H., Geller H. M., and, Symes A. J., (2014) Temporal patterns of cortical proliferation of glial cell populations after traumatic brain injury in mice. ASN Neuro. 6, 159-170.
42. Vinet J., Weering H. R., Heinrich A., Kälin R. E., Wegner A., Brouwer N., and, Heppner F. L., (2012) Rooijen Nv, Boddeke HW, Biber K. J Neuroprotective function for ramified microglia in hippocampal excitotoxicity. J. Neuroinflammation 9, 27.
43. Wang J., Gusti V., Saraswati A., and, Lo D. D., (2011) Convergent and divergent development among M cell lineages in mouse mucosal epithelium. J. Immunol. 187, 5277-5285.