Intravitreal Injection of the Attenuated Pseudorabies Virus PRV Bartha Results in Infection of the Hamster Suprachiasmatic Nucleus only by Retrograde Transsynaptic Transport via Autonomic Circuits

Journal of Neuroscience

Volumn 22, Issue 7, 2002, Pages 2701-2710

  Pickard, Gary E ^a   Smeraski, Cynthia A ^a   Tomlinson, Christine C ^a   Banfield, Bruce W ^b   Kaufman, Jessica ^a   Wilcox, Christine L ^a   Enquist, Lynn W ^c   Sollars, Patricia J ^a  

^a Department of Environmental and Radiological Health Sciences   (United States)

^b UNIVERSITY OF COLORADO   (United States)

^c PRINCETON UNIVERSITY   (United States)

Author keywords

Edinger Westphal nucleus; Olivary pretectal nucleus; PRV Bartha; Pseudorabies virus; Suprachiasmatic nucleus; Trans synaptic transport

Indexed keywords

GREEN FLUORESCENT PROTEIN; PHOTOPROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTERIOR HYPOTHALAMUS; ARTICLE; AUTONOMIC NERVE; BRAIN NUCLEUS; CELL LABELING; CONTROLLED STUDY; ENUCLEATION; EYE INFECTION; GENICULATE BODY; HAMSTER; MALE; NONHUMAN; OLIVARY NUCLEUS; PRETECTUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; PSEUDORABIES HERPETOVIRUS; SUPRACHIASMATIC NUCLEUS; SYNAPTIC TRANSMISSION; VIRUS INFECTION; VIRUS RECOMBINANT; VIRUS STRAIN; VIRUS TRANSMISSION; ANIMAL; AUTONOMIC NERVOUS SYSTEM; DISEASE COURSE; GENETICS; GROWTH, DEVELOPMENT AND AGING; NERVE CELL; NERVE FIBER TRANSPORT; PATHOLOGY; PHYSIOLOGY; PSEUDORABIES; REPORTER GENE; RETINA GANGLION CELL; SYNAPSE; SYRIAN HAMSTER; TRANSPORT AT THE CELLULAR LEVEL; VIROLOGY; VISUAL SYSTEM; VITREOUS BODY;

ANIMALS; AUTONOMIC NERVOUS SYSTEM; AXONAL TRANSPORT; BIOLOGICAL TRANSPORT; CRICETINAE; DISEASE PROGRESSION; EYE ENUCLEATION; GENES, REPORTER; HERPESVIRUS 1, SUID; LUMINESCENT PROTEINS; MESOCRICETUS; NEURONS; PSEUDORABIES; RETINAL GANGLION CELLS; SUPRACHIASMATIC NUCLEUS; SYNAPSES; VISUAL PATHWAYS; VITREOUS BODY;

EID: 0036550997     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.22-07-02701.2002     Document Type: Article

References (73)

1. Aston-Jones G, Chen S, Zhu Y, Oshinsky ML (2001) A neural circuit for circadian regulation of arousal. Nat Neurosci 4:732-738.
2. Banfield BW, Yap GS, Knapp AC, Enquist LW (1998) A chicken embryo eye model for the analysis of alphaherpesvirus neuronal spread and virulence. J Virol 72:4580-4588.
3. Billig I, Foris JM, Enquist LW, Card JP, Yates BJ (2000) Definition of neuronal circuitry controlling the activity of phrenic and abdominal motoneurons in the ferret using recombinant strains of pseudorabies virus. J Neurosci 20:7446-7454.
4. Blanks RH, Clarke RJ, Lui F, Giolli RA, Van Pham S, Torigoe Y (1995) Projections of the lateral terminal accessory optic nucleus of the common marmoset (Callithrix jacchus). J Comp Neurol 354:511-532.
5. Brideau AD, Eldridge MG, Enquist LW (2000) Directional transneuronal infection by pseudorabies virus is dependent on an acidic internalization motif in the Us9 cytoplasmic tail. J Virol 74:4549-4561.
6. Buijs RM, Markman M, Nunes-Cardoso B, Hou Y-X, Shinn S (1993) Projections of the suprachiasmatic nucleus to stress-related areas in the rat hypothalamus: a light and electron microscopic study. J Comp Neurol 335:42-54.
7. Buijs RM, Wortel J, van Heerikhuize JJ, Feenstra MG, Ter Horst GJ, Romijn HJ, Kalsbeek A (1999) Anatomical and functional demonstration of a multisynaptic suprachiasmatic nucleus adrenal (cortex) pathway. Eur J Neurosci 11:1535-1544.
8. Buijs RM, Chun SJ, Niijima A, Romijn HJ, Nagai K (2001) Parasympathetic and sympathetic control of the pancreas: a role for the suprachiasmatic nucleus and other hypothalamic centers that are involved in the regulation of food intake. J Comp Neurol 431:405-423.
9. Campbell G, Lieberman AR (1985) The olivary pretectal nucleus: experimental anatomical studies in the rat. Philos Trans R Soc Lond B Biol Sci 310:573-609.
10. Card JP (1998) Exploring brain circuitry with neurotropic viruses: new horizons in neuroanatomy. Anat Rec 253:176-185.
11. Card JP, Rinaman L, Schwaber JS, Miselis RR, Whealy ME, Robbins AK, Enquist LW (1990) Neurotropic properties of pseudorabies virus: uptake and transneuronal passage in the rat central nervous system. J Neurosci 10:1974-1994.
12. Card JP, Whealy ME, Robbins AK, Moore RY, Enquist LW (1991) Two alpha-herpesvirus strains are transported differentially in the rodent visual system. Neuron 6:957-969.
13. Card JP, Levitt P, Enquist LW (1998) Different patterns of neuronal infection after intracerebral injection of two strains of pseudorabies virus. J Virol 72:4434-4441.
14. Chen S, Yang M, Miselis RR, Aston-Jones G (1999) Characterization of transsynaptic tracing with central application of pseudorabies virus. Brain Res 838:171-183.
15. Clarke RJ, Ikeda H (1985a) Luminance detectors in the olivary pretectal nucleus and their relationship to the pupillary light reflex in the rat. II. Studies using sinusoidal light. Exp Brain Res 59:83-90.
16. Clarke RJ, Ikeda H (1985b) Luminance and darkness detectors in the olivary and posterior pretectal nuclei and their relationship to the pupillary light reflex in the rat. I. Studies with steady luminance levels. Exp Brain Res 57:224-232.
17. Daniels D, Miselis RR, Flanagan-Cato LM (1999) Central neuronal circuit innervating the Iordosis-producing muscles defined by transneuronal transport of pseudorabies virus. J Neurosci 19:2823-2833.
18. Demmin GL, Clase AC, Randall JA, Enquist LW, Banfield BW (2001) Insertions in the gG gene of pseudorabies virus reduce expression of the upstream Us3 protein and inhibit cell-to-cell spread of virus infection. J Virol 75:10856-10869.
19. Enquist LW, Dubin J, Whealy ME, Card JP (1994) Complementation analysis of pseudorabies virus gE and gI mutants in retinal ganglion cell neurotropism. J Virol 68:5275-5279.
20. Enquist LW, Husak PJ, Banfield BW, Smith GA (1999) Infection and spread of alphaherpesviruses in the nervous system. Adv Virus Res 51:237-347.
21. Gamlin PD, Reiner A, Karten HJ (1982) Substance P-containing neurons of the avian suprachiasmatic nucleus project directly to the nucleus of Edinger-Westphal. Proc Natl Acad Sci USA 79:3891-3895.
22. Gamlin PD, Zhang H, Clarke RJ (1995) Luminance neurons in the pretectal olivary nucleus mediate the pupillary light reflex in the rhesus monkey. Exp Brain Res 106:169-176.
23. Hallbeck M, Larhammar D, Blomqvist A (2001) Neuropeptide expression in rat paraventricular hypothalamic neurons that project to the spinal cord. J Comp Neurol 433:222-238.
24. Holstege G (1987) Some anatomical observations on the projections from the hypothalamus to brainstem and spinal cord: an HRP and autoradiographic tracing study in the cat. J Comp Neurol 260:98-126.
25. Husak PJ, Kuo T, Enquist LW (2000) Pseudorabies virus membrane proteins gI and gE facilitate anterograde spread of infection in projection-specific neurons in the rat. J Virol 74:10975-10983.
26. Itaya SK, Van Hoesen GV (1982) WGA-HRP as a transneuronal marker in the visual pathways of monkey and rat. Brain Res 236:199-204.
27. Jansen AS, Nguyen XV, Karpitskiy V, Mettenleiter TC, Loewy AD (1995) Central command neurons of the sympathetic nervous system: basis of the fight-or-flight response. Science 270:644-646.
28. Jasmin L, Burkey AR, Card JP, Basbaum A.I. (1997) Transneuronal labeling of a nociceptive pathway, the spino-(trigemino-)parabrachio-amygdaloid, in the rat. J Neurosci 17:3751-3765.
29. Kalsbeek A, Teclemariam-Mesbah R, Pevet P (1993) Efferent projections of the suprachiasmatic nucleus in the golden hamster (Mesocricetus auratus). J Comp Neurol 332:293-314.
30. Klooster J, Vrensen GF, Muller LJ, van der Want JJ (1995) Efferent projections of the olivary pretectal nucleus in the albino rat subserving the pupillary light reflex and related reflexes. A light microscopic tracing study. Brain Res 688:34-46.
31. Kucera P, Favrod P (1979) Suprachiasmatic nucleus projection to mesencephalic central grey in the woodmouse (Apodemus sylvaticus L.). Neuroscience 4:1705-1715.
32. la Fleur SE, Kalsbeek A, Wortel J, Buijs RM (2000) Polysynaptic neural pathways between the hypothalamus, including the suprachiasmatic nucleus, and the liver. Brain Res 871:50-56.
33. Larsen PJ, Enquist LW, Card JP (1998) Characterization of the multisynaptic neuronal control of the rat pineal gland using viral transneuronal tracing. Eur J Neurosci 10:128-145.
34. Leak RK, Moore RY (2001) Topographic organization of suprachiasmatic nucleus projection neurons. J Comp Neurol 433:312-334.
35. Levatte MA, Mabon PJ, Weaver LC, Dekaban GA (1998) Simultaneous identification of two populations of sympathetic preganglionic neurons using recombinant herpes simplex virus type 1 expressing different reporter genes. Neuroscience 82:1253-1267.
36. Levine JD, Zhao X-S, Miselis RR (1994) Direct and indirect retinohypothalamic projections to the supraoptic nucleus in the female albino rat. J Comp Neurol 341:214-224.
37. Loewy AD (1998) Viruses as transneuronal tracers for defining neural circuits. Neurosci Biobehav Rev 22:679-684.
38. Lomniczi B, Watanabe S, Ben Porat T, Kaplan AS (1987) Genome location and identification of functions defective in the Bartha vaccine strain of pseudorabies virus. J Virol 61:796-801.
39. Luiten PGM, ter Horst GJ, Karst H, Steffens AB (1985) The course of paraventricular hypothalamic efferents to autonomic structures in medulla and spinal cord. Brain Res 329:374-378.
40. Marson L (1997) Identification of central nervous system neurons that innervate the bladder body, bladder base, or external urethral sphincter of female rats: a transneuronal tracing study using pseudorabies virus. J Comp Neurol 389:584-602.
41. Mettenleiter T (1994) Pseudorabies (Aujeszky's disease) virus: state of the art. Acat Vet Hung 42:153-177.
42. Mettenleiter TC, Lukacs N, Rziha HJ (1985) Pseudorabies virus avirulent strains fail to express a major glycoprotein. J Virol 56:307-311.
43. Moore RY, Speh JC, Card JP (1995) The retinohypothalamic tract originates from a distinct subset of retinal ganglion cells. J Comp Neurol 352:351-366.
44. Moore RY, Weis R, Moga MM (2000) Efferent projections of the intergeniculate leaflet and the ventral lateral geniculate nucleus in the rat. J Comp Neurol 420:398-418.
45. Morin LP, Blanchard JH (1993) Organization of the hamster paraventricular hypothalamic nucleus. J Comp Neurol 332:341-357.
46. Morin LP, Blanchard JH (1998) Interconnections among nuclei of the subcortical visual shell: the intergeniculate leaflet is a major constituent of the hamster subcortical visual system. J Comp Neurol 396:288-309.
47. Morin LP, Wood RI (2001) A stereotaxic atlas of the golden hamster brain. New York: Academic.
48. O'Donnell P, Lavin A, Enquist LW, Grace AA, Card JP (1997) Interconnected parallel circuits between rat nucleus accumbens and thalamus revealed bv retrograde trans-synaptic transport of pseudorabies virus. J Neurosci 17:2143-2167.
49. Oyster CW (1999) The human eye. Sunderland, MA: Sinauer.
50. Perez Fontan JJ, Velloff CR (1997) Neuroanatomic organization of the parasympathetic bronchomotor system in developing sheep. Am J Physiol 273:R121-R133.
51. Petrovskis EA, Timmins J, Gierman T, Post L (1986) Deletions in vaccine strains of pseudorabies virus and their effect on synthesis of glycoprotein gp63. J Virol 60:1166-1169.
52. Pickard GE (1982) The afferent connections of the suprachiasmatic nucleus of the golden hamster with emphasis on the retinohypothalamic projection. J Comp Neurol 211:65-83.
53. Pickard GE (1985) Bifurcating axons of retinal ganglion cells terminate in the hypothalamic suprachiasmatic nucleus and the intergeniculate leaflet of the thalamus. Neurosci Lett 55:211-217.
54. Pickard GE, Card JP, Moore RY, Weeks J (1992) Pseudorabies virus labeling of the suprachiasmatic nucleus and intergeniculate leaflet in the golden hamster. Soc Res Biol Rhythms 3:64.
55. Pickard GE, Tomlinson CC, Smeraski CA, Wilcox CL, Banfield BW, Enquist LW, Sollars PJ (2001) PRV Bartha infects the suprachiasmatic nucleus in rodents via transneuronal spread through retrograde circuitry. Soc Neurosci Abstr 31:91.
56. Provencio I, Cooper HM, Foster RG (1998) Retinal projections in mice with inherited retinal degeneration: implications for circadian photoentrainment. J Comp Neurol 395:417-439.
57. Ranson SW, Magoun HW (1933) The central path of the pupilloconstrictor reflex in response to light. Arch Neurol Psychiatry 30:1193-1204.
58. Saper CB, Loewy AD, Swanson LW, Cowan WM (1976) Direct hypothalamo-autonomic connections. Brain Res 117:305-312.
59. Scalia F (1972) The termination of retinal axons in the pretectal region of mammals. J Comp Neurol 145:223-257.
60. Smith BN, Banfield BW, Smeraski CA, Wilcox CL, Dudek FE, Enquist LW, Pickard GE (2000) Pseudorabies virus expressing enhanced green fluorescent protein: a tool for in vitro electrophysiological analysis of transsynaptically labeled neurons in identified central nervous system circuits. Proc Natl Acad Sci USA 97:9264-9269.
61. Smith KC (1997) Herpesviral abortion in domestic animals. Vet J 153:253-268.
62. Strack AM, Loewy AD (1990) Pseudorabies virus: a highly specific transneuronal cell body marker in the sympathetic nervous system. J Neurosci 10:2139-2147.
63. Swanson LW (1977) Immunohistichemical evidence for a neurophysin-containing autonomic pathway arising in the paraventricular nucleus of the hypothalamus. Brain Res 128:346-353.
64. Teclemariam-Mesbah R, Kalsbeek A, Pevet P, Buijs RM (1997) Direct vasoactive intestinal polypeptide-containing projection from the suprachiasmatic nucleus to spinal projecting hypothalamic paraventricular neurons. Brain Res 748:71-76.
65. Tomishima MJ, Enquist LW (2001) A conserved α-herpesvirus protein necessary for axonal localization of viral membrane proteins. J Cell Biol 154:741-752.
66. Ueyama T, Krout KE, Nguyen XV, Karpitskiy V, Kollert A, Mettenleiter TC, Loewy AD (1999) Suprachiasmatic nucleus: a central autonomic clock. Nat Neurosci 2:1051-1053.
67. Valentino RJ, Kosboth M, Colflesh M, Miselis RR (2000) Transneuronal labeling from the rat distal colon: anatomic evidence for regulation of distal colon function by a pontine corticotropin-releasing factor system. J Comp Neurol 417:399-414.
68. Watts AH (1991) The efferent projections of the suprachiasmatic nucleus: anatomical insights into the control of circadian rhythms. In: Suprachiasmatic nucleus: the mind's eye (Klein DC, Moore RY, Reppert SM, eds), pp 77-106. New York: Oxford UP.
69. Watts AG, Swanson LW, Sanchez-Watts G (1987) Efferent projections of the suprachiasmatic nucleus: I. Studies using anterograde transport of Phaseolus vulgaris leucoagglutinin in the rat. J Comp Neurol 258:204-229.
70. Whealy ME, Card JP, Robbins AK, Dubin JR, Rziha HJ, Enquist LW (1993) Specific pseudorabies virus infection of the rat visual system requires both gI and gp63 glycoproteins. J Virol 67:3786-3797.
71. Young MJ, Lund RD (1994) The anatomical substrates subserving the pupillary light reflex in rats: origin of the consensual pupillary response. Neuroscience 62:481-496.
72. Young MJ, Lund RD (1998) The retinal ganglion cells that drive the pupilloconstrictor response in rats. Brain Res 787:191-202.
73. Zheng J-Q, Seki M, Hayakawa T, Ito H, Zyo K (1995) Descending projections from the paraventricular hypothalamic nucleus to the spinal cord: anterograde tracing study in the rat. Okajimas Folia Anat Jpn 72:119-136.