JEB Classics by shuifanglj

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									JEB Classics
 192
                                              A WIGGLESWORTH                                a subject that was pursued by perhaps
       JEB Classics is an occasional          CLASSIC: HOW CELLS                            10–20 people in the world at that time.
       column, featuring historic                                                           Pattern formation had really been
       publications from The Journal of
                                              MAKE PATTERNS                                 recognised as a specific problem by
       Experimental Biology. These                                                          German embryologists and was a straight
       articles, written by modern experts                                                  translation of their word Musterbildung.
       in the field, discuss each classic                                                    How were the tissues of an animal
       paper’s impact on the field of                                                        marshalled and directed so that they could
       biology and their own work. A                                                        construct the body? VBW realised the
       PDF of the original paper                                                            advantages offered by the insect epidermis.
       accompanies each article, and                                                        At a time when most were concerned with
       can be found on the journal’s                                                        abstract embryological concepts such as
       website as supplemental data.                                                        fields and competence, morphollaxis and
                                                                                            epimorphosis, VBW saw clearly an
                                                                                            elemental truth. In his 1940 publication, he
                                                                                            argues that patterns derive from the diverse
                                                                                            behaviour of single cells — “the tiny
                                                                                            fragment of cuticle laid down by a single
                                                                                            cell may possess morphological characters
                                                                                            controlled by the activity of that cell
                                                                                            alone”. He harnessed this hypothesis to his
                                                                                            knowledge that the insect epidermis is a
                                                                                            monolayer and was set to make his
                                                                                            observations and use his head.
                  JEB Classics

                                                                                            Scientists find their questions from
                                                                                            different sources and many, too many I
                                              Peter Lawrence writes about                   think, look in the literature, they listen into
                                              V. B. Wigglesworth’s 1940 publication         the gossip of the day and deal therefore
                                              ‘Local and general factors in the             with fashionable concerns. There is another
                                              development of ‘pattern’ in Rhodnius          way, and this is the route followed by
                                              prolixus (Hemiptera)’. A pdf file of           VBW. He let the material ask the
                                              Wigglesworth’s paper can be accessed as       questions. Looking carefully at Rhodnius
                                              supplemental data at jeb.biologists.org       he noted many features: the sensory
                                                                                            bristles, the pattern of pigment and the
                                              In January 1940, London was not the most      muscle insertions. He thought about the
                                              peaceful place in the world, but it was in    cuticular pigmentation; for example, was
                                              that month that V. B. Wigglesworth, known     something indelible written into the cells
                                              to entomologists as VBW, submitted one of     that secreted it — would they carry the
                                              his best papers to The Journal of             potential to make pigment if they were
                                              Experimental Biology. VBW was an              forced to divide? In the manner of J.-H.
                                              exceptional scientist in many ways. He was    Fabre, he intervened in a simple and direct
                                              original, reflective and a superb              way to answer the question. Early in the
                                              experimentalist, and made the field of         1940 paper, he describes how he burnt the
                                              insect physiology almost single handed. He    cells located nearby to a pigment spot,
                                              published 264 papers (all but a few, single   forcing the pigmented cells to divide as
                                              author works) and wrote 9 books               they migrated in to heal the wound. When
                                              (including the renowned work, The             the next cuticle was laid down, he found
                                              Principles of Insect Physiology) in a long    the pigment spot to be enlarged and
                                              life (Lawrence and Locke, 1997; Locke,        deformed, arguing that the pigmented cells
                                              1994). He was not a salesman — yet he         were determined and had handed on their
                                              wrote his papers in a simple and direct       state to their daughter cells.
                                              style that a first year student could
                                              understand. It is hard to think of anyone     Why are the adult and juvenile patterns so
                                              who was more unlike most successful           different? VBW had already discovered
                                              modern scientists, yet who made so many       juvenile hormone, and he knew that this
                                              important discoveries. This paper, ‘Local     hormone acted as a switch; if it was
                                              and general factors in the development of     present juvenile structures were made, if
                                              ‘pattern’ in Rhodnius prolixus (Hemiptera)’   absent then the adult pattern. Were all cells
                                              (Wigglesworth, 1940), epitomises what was     capable of responding to the hormone, or
                                              unique about his scientific approach.          did they have to be primed? VBW took
                                                                                            grafts of epidermis from younger larvae
                                              He was working on Rhodnius, a blood-          and transplanted them onto
                                              sucking bug (Hemiptera, Reduviidae) and       metamorphosing nymphs; he also moved
                                              decided to think about ‘pattern formation’,   them from place to place. He concluded

                                         THE JOURNAL OF EXPERIMENTAL BIOLOGY 207 (2)
                                                                                                                   JEB Class ics
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that cells in different places were already      spaces between the pre-existing ones. By a    Locke compared him to a type of butterfly
differently determined in respect of both        series of simple experiments and logical      that has only been seen once:
larval and adult pattern.                        deductions he concluded that the important    “Wigglesworth was just such a unique
                                                 variable was not the distance between pre-    specimen. His achievements came from a
He also noted that one moult after a burn,       existing bristles, but the number of cells.   man, a time and an opportunity that can
the bristles were missing, but in the next       How was the number of cells to be             never be repeated” (Locke, 1994). But his
moult they were regenerated. He                  measured? Here VBW proposed a                 approach can be instructive; read this 1940
commented: “It is worth noting that, with        “working hypothesis” in which a gradient      paper and learn that the material you study
few exceptions, the regenerated… bristles        molecule would be made by all the             can be a better guide at suggesting original
show the normal orientation. This raises a       epidermal cells; it would be absorbed by      questions than a visit to the library.
new problem which has not been further           pre-existing bristles but be necessary for    10.1242/jeb.00775
investigated”. He later thought about planar     engendering new ones; its concentration
polarity a little more (Wigglesworth, 1959)      would only be sufficient to sponsor new                             Peter Lawrence
but did not return to it again. Perhaps          bristles at sites far away from the others.     MRC Laboratory of Molecular Biology,
wisely, because it is still a mystery; even      He was fully aware that his simple idea                                 Cambridge
now we still don’t know what a bristle cell      could be the basis of a more general and                    pal@mrc-lmb.cam.ac.uk
reads to tell it where anterior is. VBW          molecular model of positional information
made a door-opening observation, there is        (a term to be coined in 1969; Wolpert,        Lawrence, P. A. (2001). Morphogens: how big
an interesting room behind it, but, still, 63    1969) and he compared it to models of         is the big picture? Nat. Cell Biol. 3, E151-154.
                                                                                               Lawrence, P. A. and Locke, M. (1997). A man
years on, there is too little light to see       pattern formation in hydroids and worms.      for our season. Nature 386, 757-758.
inside.                                          Indeed Morgan had proposed the idea of a      Locke, M. (1994). Professor Sir Vincent B.
                                                 morphogen much earlier (Morgan, 1897),        Wigglesworth, CBE, MD, FRS (1899–1994). J.
Next, he turned his attention to something       although his model was different to how       Insect Physiol. 40, 823-826.
else: he noticed that the bristles were          we look at morphogens now (Lawrence,          Morgan, T. H. (1897). Regeneration in
evenly spaced. Because the bristles              2001). VBW’s observations were also the       Allolobophora fœtida. Archives für
reappeared de novo after a burn he deduced       beginning of studies that led to              Entwicklungsmechanism der Organismen 5, 570-
                                                                                               586.
that epidermal cells were transforming           understanding of lateral inhibition, the      Stossberg, M. (1937). Über die Entwicklung der
themselves into bristles, a conclusion that      function of Notch and much besides.           Schmetterlingsschuppen (Untersuchungen an
fitted well with the work going on at that                                                      Ephestia kühniella Z.). Biol. Zbl 57, 393-402.
time in Germany about the development of         I don’t think VBW would have relished         Wigglesworth, V. B. (1940). Local and general
scales in moths (I think the earliest paper      reading the current literature, even those    factors in the development of ‘pattern’ in
on the scale cell lineage is Stossberg,          many papers that contain both ideas and       Rhodnius prolixus (hemiptera). J. Exp. Biol. 17,
1937). The accuracy of the spacing               data that followed from his observations.     180-200.
suggested that the epidermal cells are           Although he read enormously and was           Wigglesworth, V. B. (1959). The Control of
                                                                                               Growth and Form: A Study of the Epidermal
sensitive to their position relative to extant   encyclopaedic in his knowledge he did not     Cell in an Insect. Cornell: Cornell University
bristles. Looking at normal development he       enjoy papers that had to be decoded before    Press.
found that, as the insect grows, new bristles    they could be understood, nor did he think    Wolpert, L. (1969). Positional information and
are added, and again they are not added at       it proper for scientists to advertise         the spatial pattern of cellular differentiation. J.
random but tend to appear in the largest         themselves, or steal credit from others.      Theor. Biol. 25, 1-47.




                                          THE JOURNAL OF EXPERIMENTAL BIOLOGY 207 (2)

								
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