Chromatic organization of cone photoreceptors in the retina of rainbow trout: single cones irreversibly switch from UV (SWS1) to blue (SWS2) light sensitive opsin during natural development

Cheng, Christiana L.; Flamarique, Inĩgo Novales

doi:10.1242/jeb.009217

Cited by 77 publications

(124 citation statements)

References 45 publications

(106 reference statements)

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“…Opsin switches in postmitotic photoreceptors are well known in the developing mammalian retina, with ultraviolet/blue (SWS1) opsin expression preceding green (MWS/LWS) opsin expression (Szél et al, 1994;Cornish et al, 2004) and have been observed, during metamorphosis, in the larval eye of the fruit fly (Sprecher and Desplan, 2008) and in young fish (Gan and Novales Flamarique, 2010; references therein). In the retina of juvenile salmonids (alevin and parr stages), for example, "single cones" undergo a TH-induced switch in opsin expression from ultraviolet (SWS1) to blue (SWS2) opsin (Cheng and Flamarique, 2007;Cheng et al, 2009), with the expression levels of thyroid receptor isoforms TR␣ and TR␤ raising after developmental or experimentally induced surges in thyroid hormone (Raine and Hawryshyn, 2009;Gan and Novales Flamarique, 2010;Raine et al, 2010). In adult mammals, comparable opsin shifts have not been described, except minor circadian oscillations of opsin transcript levels (von Schantz et al, 1999), which are thought not to alter the spectral phenotype of the photoreceptor.…”

Section: Discussionmentioning

confidence: 99%

Thyroid Hormone Controls Cone Opsin Expression in the Retina of Adult Rodents

Glaschke¹,

Weiland²,

Turco³

et al. 2011

J. Neurosci.

102

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Mammalian retinas display an astonishing diversity in the spatial arrangement of their spectral cone photoreceptors, probably in adaptation to different visual environments. Opsin expression patterns like the dorsoventral gradients of short-wave-sensitive (S) and middle-to long-wave-sensitive (M) cone opsin found in many species are established early in development and thought to be stable thereafter throughout life. In mouse early development, thyroid hormone (TH), through its receptor TR␤2, is an important regulator of cone spectral identity. However, the role of TH in the maintenance of the mature cone photoreceptor pattern is unclear. We here show that TH also controls adult cone opsin expression. Methimazole-induced suppression of serum TH in adult mice and rats yielded no changes in cone numbers but reversibly altered cone patterns by activating the expression of S-cone opsin and repressing the expression of M-cone opsin. Furthermore, treatment of athyroid Pax8 Ϫ/Ϫ mice with TH restored a wild-type pattern of cone opsin expression that reverted back to the mutant S-opsin-dominated pattern after termination of treatment. No evidence for cone death or the generation of new cones from retinal progenitors was found in retinas that shifted opsin expression patterns. Together, this suggests that opsin expression in terminally differentiated mammalian cones remains subject to control by TH, a finding that is in contradiction to previous work and challenges the current view that opsin identity in mature mammalian cones is fixed by permanent gene silencing.

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Section: Discussionmentioning

confidence: 99%

Thyroid Hormone Controls Cone Opsin Expression in the Retina of Adult Rodents

Glaschke¹,

Weiland²,

Turco³

et al. 2011

J. Neurosci.

102

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“…In our previous studies, these riboprobes crosshybridized with their target opsin transcripts in other salmonid species, such as rainbow trout, and produced labeling patterns identical to those obtained with rainbow trout probes (Cheng and Novales Flamarique, 2007;. To enable simultaneous immunodetection in double in situ hybridizations, the UV riboprobe was conjugated to fluorescein (Roche Applied Sciences) and the blue riboprobe to Digoxigenin (Dig; Roche Applied Sciences).…”

Section: Opsin Riboprobe Preparationmentioning

confidence: 93%

“…In the retina of rainbow trout parr, quantitative RT-PCR analyses have shown that TRa and TRb transcription is up-regulated following 3 days of exogenous thyroid hormone exposure (Raine and Hawryshyn, 2009). This up-regulation is most pronounced in the dorso-temporal retina, the only area with a remaining population of UV opsin-expressing cones at this stage in the animal's life cycle (Cheng and Novales Flamarique, 2007;Cheng et al, , 2009. It is unknown whether the reported changes in TRb can be attributed solely to single cones, or whether they are due to variations in expression in other retinal cells (see Mader and Cameron, 2006;Trimarchi et al, 2008).…”

Section: Tra May Regulate the Uv-toblue Opsin Switch In Differentiatementioning

confidence: 99%

Thyroid hormone accelerates opsin expression during early photoreceptor differentiation and induces opsin switching in differentiated TRα‐expressing cones of the salmonid retina

Gan

Flamarique

2010

Developmental Dynamics

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Thyroid hormone and its receptors (TRs) regulate photoreceptor differentiation and visual pigment protein (opsin) expression in the retinas of several vertebrates, including rodents and fish. In some of these animals, opsin expression can arise through switches within differentiated cone photoreceptors. In salmonid fishes, single cones express ultraviolet (SWS1) opsin during embryonic development and switch to blue (SWS2) opsin as the fishes grow. It is unknown whether thyroid hormone regulates opsin expression during early cone differentiation and acts through TRs to induce opsin switches in differentiated cones of the salmonid retina. Using in situ hybridization, we characterized the spatiotemporal dynamics of opsin expression and switching in embryos treated with exogenous thyroid hormone or propylthiouracil (PTU), a pharmacological inhibitor of thyroid hormone synthesis. We combined immunohistochemistry with in situ hybridization to map TRa expression with respect to cones undergoing the opsin switch in older juvenile fish. Thyroid hormone accelerated opsin expression in differentiating cones and induced the opsin switch in differentiated single cones, whereas PTU repressed the opsin switch. TRa was not detected in differentiating photoreceptors as opsin expression initiated, but was later expressed in differentiated single cones before the onset of the opsin switch. TRa expression exhibited a dynamic dorsoventral distribution that paralleled the progression of the opsin switch. Together, our results show that thyroid hormone is required for opsin switching in the retina of salmonid fishes and suggest that TRa may be involved in regulating this phenomenon. Developmental Dynamics 239:2700-2713,

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“…However, changes in opsin expression were subsequently implicated in a number of species such as the pollack (Shand et al, 1988), goatfish (Shand, 1993) and flounder (Evans et al, 1993), and were shown to account for the blue-green sensitivity shift in the rods of the eel (Archer et al, 1995;Hope et al, 1998 Chinen et al, 2003;Takechi and Kawamura, 2005), Pacific pink salmon (Cheng and Novales Flamarique, 2004), rainbow trout (Veldhoen et al, 2006;Cheng and Novales Flamarique, 2007) and cichlids (Spady et al, 2006). A recent microspectrophotometric study of the black bream Acanthopagrus butcheri revealed a changing pattern of cone photoreceptors with different λ max values in fish at different developmental ages (Shand et al, 2002).…”

Section: Introductionmentioning

confidence: 99%

The influence of ontogeny and light environment on the expression of visual pigment opsins in the retina of the black bream,Acanthopagrus butcheri

Shand

Davies²,

Thomas

et al. 2008

Journal of Experimental Biology

132

140

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SUMMARYThe correlation between ontogenetic changes in the spectral absorption characteristics of retinal photoreceptors and expression of visual pigment opsins was investigated in the black bream, Acanthopagrus butcheri. To establish whether the spectral qualities of environmental light affected the complement of visual pigments during ontogeny, comparisons were made between fishes reared in: (1) broad spectrum aquarium conditions; (2) short wavelength-reduced conditions similar to the natural environment; or (3) the natural environment (wild-caught). Microspectrophotometry was used to determine the wavelengths of spectral sensitivity of the photoreceptors at four developmental stages: larval, post-settlement, juvenile and adult. The molecular sequences of the rod (Rh1) and six cone (SWS1, SWS2A and B, Rh2Aα and β, and LWS) opsins were obtained and their expression levels in larval and adult stages examined using quantitative RT-PCR. The changes in spectral sensitivity of the cones were related to the differing levels of opsin expression during ontogeny. During the larval stage the predominantly expressed opsin classes were SWS1, SWS2B and Rh2Aα, contrasting with SWS2A, Rh2Aβ and LWS in the adult. An increased proportion of long wavelength-sensitive double cones was found in fishes reared in the short wavelength-reduced conditions and in wildcaught animals, indicating that the expression of cone opsin genes is also regulated by environmental light.

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Chromatic organization of cone photoreceptors in the retina of rainbow trout: single cones irreversibly switch from UV (SWS1) to blue (SWS2) light sensitive opsin during natural development

Cited by 77 publications

References 45 publications

Thyroid Hormone Controls Cone Opsin Expression in the Retina of Adult Rodents

Thyroid Hormone Controls Cone Opsin Expression in the Retina of Adult Rodents

Thyroid hormone accelerates opsin expression during early photoreceptor differentiation and induces opsin switching in differentiated TRα‐expressing cones of the salmonid retina

The influence of ontogeny and light environment on the expression of visual pigment opsins in the retina of the black bream,Acanthopagrus butcheri

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