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(short answer, I found the cause, and a suitable monkey patch) - below are details of how I did it and steps I took.
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Okay so I forked AbstractHTTPHandler() then patched do_request_(), at which point "request.headers" and request.header_items() have the correct header name (Content-MD5).
So I tried this:
opener = urllib2.build_opener(urllib2.HTTPHandler(debuglevel=1))
opener.addheaders = [("Content-TE5", 'test'), ]
However the headers came back capitalized, so the problem is happening somewhere after addheaders. 
 > grep -R "addheaders" *.py
urllib.py: self.addheaders = [('User-Agent', self.version)]
urllib.py: self.addheaders.append(args)
urllib.py: for args in self.addheaders: h.putheader(*args)
urllib.py: for args in self.addheaders: h.putheader(*args)
urllib2.py: self.addheaders = [('User-agent', client_version)]
urllib2.py: for name, value in self.parent.addheaders:
> grep -R "def putheader" *.py
httplib.py: def putheader(self, header, value):
httplib.py: def putheader(self, header, *values):
I also then found: http://stackoverflow.com/questions/3278418/testing-urllib2-application-http-responses-loaded-from-files
I then patched this:
 class HTTPConnection(httplib.HTTPConnection):
 def putheader(self, header, value):
 print [header, value]
This in turn brought back:
['Content-Md5', 'nts0yj7AdzJALyNOxafDyA==']
Which means it's happening before putheader(). So I patched _send_request() on HTTPConnection(), and that also brought back 'Content-Md5'. Exception trace shows:
 File "/ddcms/dev/webapp/../webapp/sites/ma/management/commands/ddcms.py", line 147, in _send_request
 _res = opener.open(req)
 -- CORRECT --
 File "/usr/local/lib/python2.6/urllib2.py", line 391, in open
 response = self._open(req, data)
 -- CORRECT --
 File "/usr/local/lib/python2.6/urllib2.py", line 409, in _open
 '_open', req)
 -- CORRECT --
 File "/usr/local/lib/python2.6/urllib2.py", line 369, in _call_chain
 result = func(*args)
 -- CORRECT --
 File "/ddcms/dev/webapp/../webapp/sites/ma/management/commands/ddcms.py", line 126, in http_open
 return self.do_open(HTTPConnection, req)
 -- CORRECT --
 File "/usr/local/lib/python2.6/urllib2.py", line 1142, in do_open
 h.request(req.get_method(), req.get_selector(), req.data, headers)
 -- INVALID --
 File "/usr/local/lib/python2.6/httplib.py", line 914, in request
 self._send_request(method, url, body, headers)
 File "/ddcms/dev/webapp/../webapp/sites/ma/management/commands/ddcms.py", line 122, in _send_request
 raise
The line that causes it?
 headers = dict(
 (name.title(), val) for name, val in headers.items())
 
So it would appear that title() also needs monkey patching.. Patched to use:
# Patch case sensitive headers (due to reflected API being non RFC compliant, and
# urllib2 not giving the option to choose between the two)
class _str(str):
 def capitalize(s):
 print "capitalize() bypassed: sending value: %s" % ( s )
 return s
 
 def title(s):
 print "title() bypassed: sending value: %s" % ( s )
 return s
_headers = {_str('Content-MD5') : _md5_content}
capitalize() bypassed: sending value: Content-MD5
title() bypassed: sending value: Content-MD5
send: 'POST /url/api HTTP/1.1\r\nContent-MD5: nts0yj7AdzJALyNOxafDyA==\r\n\r\n'